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ISSN 2039-0394 (Print Edition)
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Biodiversity
Journal
DECEMBER 2014, 5 (4): 445-558
FOR NATURALISTIC RESEARCH
AND ENVIRONMENTAL STUDIES
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o n I u s
Himantopus himantopus Linnaeus, 1 758 - Italy, Sicily, Vendicari
BIODIVERSITY JOURNAL
2014,5 (4): 445-558
Quaternly scientific journal
edited by Edizioni Danaus,
viaV. Di Marco 43, 90143 Palermo, Italy
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biodiversityjournal@gmail.com
Official authorization no. 40 (28. 1 2.20 1 0)
ISSN 2039-0394 (Print Edition)
ISSN 2039-0408 (Online Edition)
Nature Reserve of Vendicari (Italy, Sicily),
landscape (photo by G. Iuvara).
Pendolino, Remiz pendulums (Linnaeus,
1758) (Seidlitz, 1 896) on the nest (photo by
G. 1 uvara). Cover: photo by Iuvara.
The Vendicari Nature Reserve (Italy, Sicily). The Oriented Natural Reserve (O.N.R.) “Oasi
faunistica di Vendicari”, in the territory of Noto (Sicily, Italy), UNESCO World Heritage City, was
established in March 1 4 ,h 1 984. Despite its small size (total of 1 335.62 acres), within the reserve there is
a concentration of environments hardly observable in other parts of Sicily. In particular, there have
been identified as habitats of interest to the European Community: Intermittently flowing
Mediterranean rivers of the Paspalo-Agrostidion (Habitat code 3290); Vegetated sea cliffs of the
Mediterranean coasts with endemic Limonium spp. (code 1240); Endemic phryganas of the
Euphorbio-Verbascion (code 5430); Thermo-Mediterranean and pre-desert scrubs (code 5330);
embryonic shifting dunes (code 2110); Shifting dunes along the shoreline with Ammophila arenaria
(white dunes) (code 2120); Coastal dunes with Juniperus spp. (code 2250, priority habitat); Coastal
lagoons (code 1150, priority habitat); Mediterranean and thermo-Atlantic halophilous scrubs
(Sarcocornetiea fruticosi ) (code 1420); Salicornia and other annuals colonizing mud and sand
(code 1310); Mediterranean salt meadows ( Juncetalia maritimi ) (code 1 4 1 0). A highly rich biodiversity
was therefore already reported for the reserve: data are contained in a compendium published in 20 10
[Petralia A. ( a cum di) 2010. L'area protetta di Vendicari. ©Ente Fauna Siciliana, Noto, Italy
(www.entefaunasiciliana.it)]. The plant list includes 486 species (48.4% therophytes, 22.0%
hemicryptophytes, 13.7% geophytes, 6.2% chamaephytes, 6.0% phanerophytes, 2.7% nano-
phanerophytes, 0.8% hydrophytes). There are 7 species of mammals, 25 1 bird species (79 of which are
included in the Directive 2009/147/EEC), 4 species of Amphibians, and 10 of Reptiles; moreover,
after decades of absence, in 20 1 3 and 20 1 4, Caretta caretta returned to the reserve for nesting. 221 are
the species of Macrolepidoptera present (24.0% of the species known for Sicily, 10.82% for Italy).
Among orthopteroids there are 32 species (including the Ensifer Brachytrupes megacephalus, species
of Community interest). As concerns the fauna of the marshes of the reserve, 22 species of molluscs, 3
of crustaceans, 2 of bristle worms (Polychaetes) and 7 of fish have been reported. More generally,
further faunistic data may be derived from a larger survey [Pi l a to et al., 2007. La fauna della regione
iblea. In "L'uomo negli Iblei" (a cura di A. Petr alia). ©Ente Fauna Siciliana, Noto, Italy
(www.entefaunasiciliana.it)] that lists 2914 species and subspecies referring to the entire iblean area
including Vendicari; of course the knowledge of fauna is periodically refreshed by new acquisitions
such as the recent discovery of the presence of the relevant beetle Buprestis cupressi (Buprestidae).
Finally, a project for the establishment of the Protected Marine Area of Vendicari aims to extend
protection also to the sea off the reserve, with its seabed equally rich in biodiversity.
Alfredo Petralia. Ente Fauna Siciliana Onlus, Noto, Italy; e-mail: alfredo.petralia@yahoo.it
Biodiversity Journal, 2014, 5 (4): 447-452
Global biodiversity gain is concurrent with declining popula
tion sizes
John C. Briggs
Oregon State University, Department of Fisheries and Wildlife, Corvallis, OR 97333, U.S.A; e-mail: clingfishes@yahoo.com
Current address: 2320 Guerneville Rd., Santa Rosa, CA 95403, U.S.A.
ABSTRACT Many authorities believe that the world’s foremost conservation problem is biodiversity loss
caused by the extinctions of thousands of species per year. Estimates of huge losses are based
on indirect evidence such as the amount of habitat destroyed, pollution, or overexploitation.
But, we now have documented records of species extinctions that provide direct instead of
indirect information about diversity loss. By using extinction records for well-known animal
groups plus surrogate data, I show there is no evidence for an unusually high rate of extinction,
a mass extinction is not yet underway, and there are indications of a continued biodiversity
gain. On the other hand, there is ample evidence to demonstrate the persistence of numerous
small populations that are the remnants of once widespread and productive species. These
populations represent an extinction debt that will be paid unless they are rescued through
present day conservation activity. They constitute the world’s true biodiversity problem.
KEY WORDS biodiversity gain; biodiversity loss; conservation; extinction debt; speciation.
Received 22.08.2014; accepted 02.11.2014; printed 30.12.2014
INTRODUCTION
As new portions of terrestrial wilderness con-
tinue to be utilized or modified by human activity,
wildlife has less territory, individual species are
crowded into smaller spaces, and many of them lose
population size until their existence becomes pre-
carious. Overexploitation by hunting and trapping
directly affect populations of birds and mammals.
In the oceans, there is loss of natural habitat over
large areas of sea bottom through the action of com-
mercial trawlers, and by the degradation of coral
reefs by human use and global warming. Along
shorelines, construction and pollution have im-
pacted much of the shallow marine habitat. The di-
rect effect of overfishing has resulted in hundreds
of species being reduced to remnants of their origi-
nal population sizes. These kinds of impacts are as-
sumed to have contributed to a global biodiversity
loss of several thousand species each year, an
apparent crisis that has been called the world’s
greatest conservation problem.
The reactions of conservation societies and gov-
ernment agencies to the foregoing problems have
tended in two directions: (1) trying to stem the per-
ceived loss of biodiversity due to species extinction,
and (2) paying attention to the plight of species that
are threatened by extinction. This brings up the
question, should we continue to concentrate on
overall biodiversity loss or should we devote more
resources to the needs of individual species? One
might say that both conservation approaches are im-
448
John C. Briggs
portant, but is this really true? Let us first consider
biodiversity loss.
BIODIVERSITY LOSS?
Global and local losses of biodiversity have
been a major focus of conservation action for 40
years. Anguish over the apparent, continuing ex-
tinction of large numbers of species has been ex-
pressed in numerous scientific papers, newspaper
and magazine articles, and on the internet. As
E.O. Wilson (1993) has noted, biodiversity, as a
term and a concept, has been a remarkable event
in recent cultural history. It was born as “BioDi-
versity” during the National Forum on BioDiver-
sity held in Washington, D.C., in September, 1986.
Prior to that time, Norman Myer’s (1979) book
had caused considerable excitement when it pre-
dicted the extinction of one million species be-
tween 1975 and 2000.
By the 1990s, numerous books and articles had
described biodiversity loss in terms of thousands of
species that disappeared each year. Among the most
notable, were A1 Gore’s (1992) book which esti-
mated that 40,000 species were disappearing each
year, and E.O. Wilson’s (1993) prediction of about
27,000 rain forest extinctions per year. Other huge
species loss estimations (Briggs, 2014) were soon
followed by declarations that the Earth had started
to undergo its sixth great mass extinction (Ceballos
et al., 2010; Kolbert, 2014).
In retrospect, biodiversity loss became rapidly
established as a scientific revelation and there
were few questions about sources of the informa-
tion. But, such concepts or theories need to be sup-
ported by facts and, in this case, the facts were few
and the theory was so captivating that it survived
even with little support for 40 years. The begin-
ning can be traced back to an influential work on
island biogeography by MacArthur & Wilson
(1967). The authors found that on small islands,
species diversity was determined by island size,
i.e., the larger the size, the greater the diversity.
Also, they found a constant turnover whereby the
numbers of invading species were balanced by the
native species that were lost. In subsequent years,
more research was done on islands and other small
habitats and these two discoveries were generally
substantiated.
The relationship between area size and species
diversity became important to many ecologists who
were convinced that, if a given amount of habitat
was destroyed, a certain number of species must be
lost. That idea was converted to a “rule of thumb”
which stated that when a habitat is reduced to one
tenth its original size, the number of species even-
tually drops to one half (Wilson, 1993). This species-
area rule (SAR) become well accepted and began
to be applied to locations ranging from small
islands to large continental areas. However, prohib-
itive difficulties became apparent when the SAR
was applied to areas larger than small, isolated
islands. As noted by Whittaker et al. (2001), the
problem with such data is one of scale. When small
scale data are applied to very large scale areas, the
results are apt to become meaningless. Furthermore,
there has been constructive criticism about the use-
fulness of the SAR (He & Hubbell, 2011). To avoid
the SAR problem, as well as to depend on direct
instead of theoretical data, it is preferable to utilize
information from documented extinctions. More
recently, various statistical methods have been used
to manipulate the theoretical extinction data in order
to prove large annual losses (for example Pimm et
al., 2014), but they unnecessarily complicate what
is actually a simple problem. By utilizing informa-
tion from recorded extinctions, together with data
from well-known surrogate taxa, I show that rate of
recent extinctions has been very low.
Documented extinctions
Until recent years, there had not been sufficient
data on species extinctions to provide an overall
estimate of biodiversity loss over the past 500 years
or more. But now, the availability of more data,
based on contemporary and fossil extinctions, has
made possible a new analysis. It is important to note
that previous estimates were made primarily on life
in the terrestrial and freshwater environments.
Obviously, global predictions should also depend
on information from the sea which covers about
71% of the Earth’s surface. There is one significant
difference between the data from land and sea. In
the first instance, there have been, in the early years
of island explorations by humans, thousands of
extinctions of endemic species that were confined
to very small spaces. But in the second case, recorded
extinctions have been remarkably few.
Global biodiversity gain is concurrent with declining population sizes
449
Although attention has been called to marine
biodiversity losses by Worm et al. (2006), that arti-
cle was referring to decreases in population size
rather than species extinction. The Holocene began
about 12,000 years ago and a total of 20 marine
extinctions were recorded by Dulvy et al. (2009).
When the losses of the 20 marine species (4 mam-
mals, 8 birds, 4 molluscs, 3 fishes, 1 alga) are com-
pared to a total marine diversity of about 2.21
million eukaryotic species (Mora et al., 2011), the
rate of extinction becomes vanishingly small.
Although it is often assumed that invasive species
are responsible for native extinctions, none of the
20 marine extinctions have been due to competition
from exotic invaders (Briggs, 2007).
In fact, there is now good evidence that invasive
species function to increase rather than decrease
biodiversity. In locations where large numbers of
exotic species are being introduced, such as the
eastern Mediterranean Sea (Galil, 2007) and in
many harbors and estuaries (Briggs, 2012), the
invaders are accommodated by the native species
resulting in local biodiversity increases. Informa-
tion from Pliocene invasions demonstrates that a
large fraction of invaders eventually speciate
(Vermeij, 1991; 2005) thus adding to global bio
diversity. It has been concluded that in the marine
environment, invader species are a dynamic diver-
sity-creation force with a circumglobal influence
(Briggs & Bowen, 2013).
In the terrestrial environment, the birds and
mammals are the best known vertebrates and their
extinction rates have been recorded. The records
and geographical locations of the extinctions, based
on evidence in the IUCN Red List and the CREO
List at the American Museum of Natural History,
have been analyzed by Loehle & Eschenbach
(2012). Extinctions during the past 500 years
demonstrate an enormous difference between
islands and continents. On all continents, only three
mammals are recorded as having gone extinct. The
remaining mammal extinctions (58 or 95%) took
place on islands (Australia, due to its history of iso-
lation, was classified as an island). Of 128 extinct
bird species, 122 (95.3%) were island extinctions
and only six were on continents. It has been ob-
served that well-known surrogate taxa can be used
as biodiversity indicators (Caro & O’ Doherty,
1999). If we use the birds and mammals as surro-
gates for all the vertebrates, this suggests that
extinction rates among the vertebrate animals of the
world’s continents have been very low. Another
discovery (Loehle & Eschenbach, 2012) was that
none of the bird and mammal extinctions were
known to have occurred solely because of habitat
reduction. For many years, habitat reduction, espe-
cially tropical deforestation, had been regarded as
the primary cause of species loss. A recent study of
the vertebrate species in the Brazilian Amazon by
Weam et al. (2012) demonstrated that extinctions
have been minimal (1%) and that 80% of the losses
predicted by habitat decline were yet to come.
For invertebrates, the Zoological Society of
London has published the world’s first study of
global invertebrate biodiversity (Collen et al.,
2012). This report, produced in conjunction with
the IUCN and its Species Survival Commission,
concluded that about 80% of the world’s species
were invertebrates and about 20% of them were
threatened with extinction. Of the world’s terrestrial
invertebrates, about 90% are insects. This suggests
if dependable information on insect extinction rates
were available, it might yield an approximate rate
for terrestrial invertebrates as a whole. Three orders
of insects: butterflies, tiger beetles, and Odonata
(dragonflies and damselflies), have been studied to
the extent that almost all the species are well
known. The world total of butterfly species is about
17,280 (Shields, 1989). Although three species are
often listed as extinct (two in South Africa and one
in the USA), the records are doubtful. Ehrlich
(1995) found that there was no documented extinc-
tion of a continental butterfly species anywhere in
the world. No island butterfly species has been
recorded to be extinct.
There are about 2,300 species of tiger beetles
(Pearson, 2001) and, although several are listed as
endangered, none has become extinct. For the
Odonata, a random sample of 1,500 of the 5,680
described species was assessed (Clausnitzer et al.,
2009). Ten percent were found to be threatened but
none of them had become extinct. In fact, there are
only two documented extinctions, one from Maui
in the Hawaiian Islands and the other from St.
Helena, an isolated island in the South Atlantic. If
the three insect orders can constitute a surrogate
group for all insects, and if the lack of extinction
among the insects (two out of 25,260) is indicative
of the terrestrial invertebrates, the extinction rate
has been exceedingly low.
450
John C. Briggs
The foregoing indications of very low extinction
rates may be compared to data that show continuing
gains in species diversity.
Biodiversity gains
While global losses were evidently minimal dur-
ing the past 400 to 500 years, there is evidence that
concurrent gains have taken place. As noted for the
marine environment, invasive species add to local
biodiversity and many of them eventually speciate,
thus increasing global diversity. Other paths to spe-
ciation have also become apparent. Molecular re-
search has revealed numerous cases of rapid
adaptive divergence resulting in ecological specia-
tion. Such cases have been demonstrated in plants,
invertebrates, and vertebrates (Hendry et al., 2007).
Specific examples have been reported in mammals
(Rowe et al., 2011), echinoderms (Puritz et al.,
2012), and plants (Foxe et al., 2009). Within the
past few centuries, species diversity has increased
on oceanic islands and in many continental regions;
furthermore, no general decreases in diversity have
been known to occur at regional scales (Sax &
Gaines, 2003).
In fact, human introductions for agricultural and
ornamental purposes, along with natural invasions,
have produced substantial gains in continental plant
biodiversity (Ellis et al., 2012). These positive
indications of biodiversity increase indicate that the
Earth is still gaining biodiversity, just as it has been
for the past 65 million years (MacLeod, 2013).
DISCUSSION
It is now possible to make a realistic assessment
of recent global biodiversity trends without having
to depend on estimates of habitat destruction,
species invasions or other abstract and possibly sub-
jective factors. For the past 500 years, there have
been few documented extinctions in the oceans or
on the continents, with the exceptions of some
restricted freshwater habitats. In using these data, I
do not imply an absence of unobserved extinctions
among groups of lesser known organisms. Even
when estimates of such extinctions are included, it
has been found that contemporary extinctions could
not have been as high as generally predicted
(Costello et al., 2013), and that less than 1% of all
organisms could have become extinct within the
past 400 years (Stork, 2010). Global projections of
biodiversity loss have generally included estimates
of extinction due to invasive species (McGeoch et
al., 2010). But, detailed studies have found no evi-
dence that invasive species are implicated in the
extinction of continental natives (Gurevitch &
Padilla, 2004; Davis, 2009).
The losses of endemic species on islands and in
freshwater lakes, while regrettable, took place on
very small spots on the Earth’s surface and their ex-
tinctions had little effect on the ecology of the main-
land biotas. Those endemics are generally
short-lived and tend to appear and disappear along
with their habitats (Whittaker et al., 2008). Of
course, there are the exceptions of a few ancient
islands and lakes that demonstrate the effects of
evolution and extinction over long time periods.
Why do small places lose species to invaders while
mainland habitats do not? The demise of almost all
island/lake endemics has been due to humans and
species they introduced (Blackburn et al., 2004).
Extinctions resulting from natural (non-human)
invaders have seldom been recorded. Despite the
early losses of endemic species, oceanic islands
have shown biodiversity gains in recent years (Sax
& Gaines, 2003).
The world’s greatest conservation problem is
exemplified by the thousands of species that were
once widespread but are now represented only by
very small populations. They are the remnants of
species that were almost destroyed by human over-
exploitation, habitat destruction and pollution.
These populations are threatened because they have
suffered genetic loss due to their reduced size,
inbreeding, and depensation (Allee effect). Genetic
loss reduces the ability to respond to environmental
change such as continued global warming. Further-
more, small populations are often confined to re-
stricted habitats, from which they would be unable
to migrate in response to climatic change. Formerly
abundant species that now exist in small numbers
are considered to be evidence of an extinction debt,
one that will be paid when environmental change
proves too difficult for them to adapt (Kuussaari et
al., 2009). If governments and conservation soci-
eties could be convinced to spend less effort on myth-
i-cal global biodiversity loss, and more on the needs
of species that are at risk, the world would have a
consolidated conservation goal that could produce
Global biodiversity gain is concurrent with declining population sizes
451
better results. The conservation plan, initiated by
the World Wildlife Fund, and supported by the Zoo-
logical Society of London, the Global Footprint
Network, and the European Space Agency, is
promising. Their Living Planet Index (2012) pro-
vided information on the status of 9,014 vertebrate
populations belonging to 2,688 species. The Index
reported that the population sizes had undergone a
28% global loss since 1970; the greatest decline
was in the tropics where the loss was 60%. The
Living Planet Index needs to be expanded to cover
invertebrates and plants.
CONCLUSIONS
In regard to the question about the need for con-
servation measures to be applied to global biodiver-
sity loss or to the precarious condition of species
that have been reduced to small populations, there
is no longer cause to be concerned about biodiver-
sity loss because it is apparently not true. For the
past 40 years, estimates of global loss, based on the
extinction of thousands of species per year, have
been a primary concern of ecologists and conserva-
tionists. These estimates, mainly due to belief in the
utility of the SAR, are shown to be erroneous and
the SAR is found to be applicable only to small
islands, lakes, and other restricted habitats. On the
other hand, we now have substantial evidence of
gains in global species diversity. This should permit
conservation societies, government entities, and
interested individuals to concentrate on species that
are at risk on the continents and in the oceans, as
well as species confined to islands and smaller
habitats. Species at risk comprise an extinction debt
that will be paid unless they are rescued before
global warming or other environmental change
takes their toll. A conservation emphasis on criti-
cally endangered species does not mean that
projects to preserve rain forests, coral reefs, and
other natural habitats should be abandoned.
On the contrary, such high diversity areas are
sources of biodiversity and are significant in an
evolutionary sense. Flowever, each species that is
at risk must be considered in view of its own con-
servation problems that are often unrelated to
habitat area. The current (2014) IUCN Red List
identifies 4,286 species that are critically endan-
gered and likely to become extinct due to global
warming or the inherent risks of small population
size. We need to be aware that many of those
species can be rescued prior to the anticipated rise
in extinctions.
ACKNOWLEDGEMENTS
I wish to thank M.A. Davis, E.A. Hanni, C.
Mora, and D.F. Sax for their help in reading and
improving the manuscript.
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Biodiversity Journal, 2014, 5 (4): 453-458
New records of sea stars (Echinodermata Asteroidea) from
Malaysia with notes on their association with seagrass beds
Woo Sau Pinn 1 *, Amelia Ng Phei Fang 2 , Norhanis Mohd Razalli 2 , Nithiyaa Nilamani 2 , Teh Chiew Peng 2 ,
ZulfigarYasin 2 , Tan Shau Hwai 2 &Toshihiko Fujita 3
'Department of Biological Science, Graduate School of Science, The University of Tokyo 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-
0033 Japan.
2 Universiti Sains Malaysia, School of Biological Sciences, Marine Science Lab, 11800 Minden, Penang, Malaysia
department of Zoology, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, Ibaraki 305-0005 Japan
Corresponding author, e-mail: abe_woo@hotmail.com
ABSTRACT A survey of sea stars (Echinodermata Asteroidea) was done on a seagrass habitat at the south-
ern coast of Peninsular Malaysia. A total of five species of sea stars from four families (Luidi-
idae, Archasteridae, Goniasteridae and Oreasteridae) and two orders (Paxillosida and
Valvatida) were observed where three of the species were first records for Malaysia. The sea
stars do not exhibit specific preference to the species of seagrass as substrate, but they were
more frequently found in the area of seagrass that have low canopy heights.
KEY WORDS Biodiversity; seagrass; sea stars; Straits of Malacca.
Received 15.09.2014; accepted 02.12.2014; printed 30.12.2014
INTRODUCTION
The knowledge of diversity and distribution of
asteroids in Malaysia is very limited. There are only
three accounts of sea stars (Echinodermata Aster-
oidea) previously reported in Malaysia where all of
the surveys are mainly done in shallow coral reefs
(George & George, 1987; Zulfigar et al., 2008; Sim
et al., 2009).
Seagrass beds are another important marine
environment in Malaysian waters. There are a
total of 14 species of seagrasses recorded (Bujang
et al., 2006), and apart from the common inshore
lagoons, seagrass meadows are also found in the
offshore islands with fringing reefs (Bujangand &
Zakaria, 2003). This study presents the first
record of asteroids associated with a seagrass bed
in Malaysia.
MATERIAL AND METHODS
A survey of sea stars was done in the seagrass
bed of Merambong shoal (N 1°19 , 58.01”; E 103°
36’ 08.30”) southern tip of Peninsular Malaysia
(Fig. 1). Wandering transect was done by walking at
seagrass bed when it was exposed extensively
during the best low spring tide of the year from 25th
to 27th of May 2013 (07:30-09:30 h). The exposure
of the seagrass bed only allowed a window of two
hours of sampling per day for three days. Asteroids
were collected using labelled sampling bags and
brought to the laboratory for further identifications.
Asteroid specimens were anaesthetized using sea-
water mixed with menthol crystals. Colour photo-
graphs of live specimens were taken before being
fixed using 70% ethanol. All specimens were
preserved by drying and deposited in Marine
454
Woo Sau Pinn et alii
Science Lab, Universiti Sains Malaysia, Penang,
Malaysia (MSL/MS).
RESULTS AND DISCUSSION
Five species of asteroids from four families and
two orders were found in the Merambong shoal sea-
grass bed: Luidia maculata of the family Luidiidae
(Fig. 9, voucher specimen MSL/MS/AST001),
Archaster typicus of Archasteridae (Figs. 2, 3 -
voucher specimen MSL/MS/AST002), Stellaster
equestris from the family Goniasteridae (Figs. 4, 5
- voucher specimen MSL/MS/AST003) and two
from family Oreasteridae: Protoreaster nodosus
(Fig. 8, voucher speciemen MSL/MS/AST004),
Goniodiscaster scaber (Figs. 6, 7 - voucher speci-
men MSL/MS/AST005).
All species of asteroids occurring in Malaysian
waters are listed in Table 1 . Previous records were
based on George & George (1987), Zulfigar et al.
(2008), and Sim et al. (2009). The areas surveyed
and covered by these three previous publications
were larger and centered at coral reefs which con-
tribute to the higher number of species of asteroids.
Zulfigar et al. (2008) and Sim et al. (2009) listed
asteroids found in shallow reefs throughout the
entire coast of Malaysia and George & George
(1987) at the lagoons and coral reefs of east coast
of Sabah. All five species were widely distributed
in Indo-West Pacific region (Clark & Rowe, 1971).
Besides their wide distribution, the present records
of Stellaster equestris , Luidia maculata and Go-
niodiscaster scaber were new state records in
Malaysian waters filling the gap in the species
distribution along the transition waters of Straits of
Malacca and South China Sea, consequently in-
creasing the total number of asteroids recorded in
Malaysian waters to 34 species. The recurring
species were Archaster typicus and Protoreaster no-
dosus , which had been both recorded in the central
of South China Sea and the East Coast of Sabah.
Protoreaster nodosus is known to prefer sub-
strates of seagrass and sand (Zulfigar et al., 2008)
even though it has been rarely found on corals and
rocks (Bos et al., 2008). Archaster typicus is found
in a wide range of sediment types which include
seagrass beds (Huang et al., 2006), and Mukai et al.
(1986) noted that the distribution of A. typicus was
independent of the specific grain size. Other species
S. equestris , L. maculata and G. scaber were com-
monly reported throughout the Indo-Pacific region
but were not specifically mentioned to be associated
with the seagrass except L. maculata on the sea-
grass of the western Arabian Gulf (Price, 1981).
Seagrass plays many important ecological func-
tions in the marine environment such as food,
1.38
Malaysia
/
/
/ 1.37
/
/
/
I
Straits of Johor
Tanjung Pelepas Port
/
/
/
/
/
/
5 km
Singapore
1.36
1.35
1.34
1.33
1.32
1.31
103.56 103.57 103.58 103.59 103.6 103.61 103.62 103.63 103.64
Figure 1. Study area in Merambong shoal, southern tip of Peninsular Malaysia in the Straits of Johor.
New records of sea stars (Asteroidea) from Malaysia with notes on their association with seagrass beds
455
Figures 2, 3. Archaester typicus : dorsal view (Fig. 2) and ventral view (Fig. 3). Figures 4, 5. Stellaster equestris : dorsal
view (Fig. 4) and ventral view (Fig. 5). Figures 6, 7. Goniodiscaster scaber. dorsal view (fig. 6) and ventral view (Fig. 7).
456
Woo Sau Pinn et alii
List of Species
George &
George, 1987
Zulfigar
et al., 2008
Sim et al., 2009
This study
ACANTHASTERIDAE
Acanthaster planci (Linnaeus, 1758)
#
#
#
ARHCASTERIDAE
Archasterty picus Muller et Troschel, 1 840
#
#
ASTEROPSE1DAE
Asteropsis carinifera (Lamarck, 1816)
#
#
ECHINASTERIDAE
Echinaster callosus Marenzeller, 1895
#
#
#
Echinaster luzonicus (Gray, 1840)
#
#
#
Echinaster sp.
#
Metrodira subulata Gray, 1 840
#
GONIASTERIDAE
Stellaster equestris (Retzius, 1805)
#*
LUIDIIDAE
Luidia maculata Muller et Troschel, 1840
#*
MITHORODIIDAE
Mithorodia fisheri Holly, 1932
#
#
OPHID1ASTER1DAE
Celerina heffernani (Livingstone, 1936)
#
Fromia elegans H.L. Clark, 1921
#
Fromia milleporella (Lamarck, 1816)
#
Fromia monilis (Perrier, 1869)
#
#
#
Fromia indica (Perrier, 1869)
#
#
Fromia sp.
#
Linckia guildingi Gray, 1 840
#
#
Linckia laevigata (Linnaeus, 1758)
#
#
#
Linkia cf. multifora (Lamarck, 1816)
#
#
#
Linckia multifora (Lamarck, 1816)
#
#
Nardoa cf. gomophia (Perrier, 1875)
#
#
Nardoa galathea (Liitken, 1865)
#
Nardoa gomophia (Perrier, 1875)
#
Nardoa tuberculata (Gray, 1 840)
#
Nardoa novaecaledoniae (Perrier, 1875)
#
Leiaster speciosus von Martens, 1866
#
#
Leiaster sp.
#
Ophidia sterhemprichi Muller et Troschel, 1842
#
#
OREASTER1DAE
Choriaster granulatus Liitken, 1869
#
#
#
Culcita novaeguineae Muller et Troschel, 1 842
#
#
#
Culcita cf. coriacea Muller et Troschel, 1 842
#
Goniodiscaster scaber (Moebius, 1 859)
#*
Neoferdina off red (Koehler, 1910)
#
#
Protoreaster nodosus (Linnaeus, 1758)
#
#
#
Pentaster obtusatus (Bory de St. Vincent, 1827)
#
Total number of species
19
20
19
5
Table 1. Records of asteroids in Malaysian (* new records found in Malaysian waters).
New records of sea stars (Asteroidea) from Malaysia with notes on their association with seagrass beds
457
refuge and habitat for numerous other associated
organisms, improving water quality and as natural
barrier for protection of coasts against wave actions,
and sea stars are one important organism associated
to the seagrass bed (Gullstrom et al., 2002). The
seagrass of Merambong shoal is composed of ten
different species of seagrasses: Enhalus acroides,
Halodule uninervis, Halodule pinifolia , Cymodocea
serrulata, Cymodocea rotundata , Thalassia
hemprichii , Halophila spinulosa, Halophila ovalis,
Halophila minor and S yringodium isoetifolium
(Bujang et al., 2006).
Field observation did not reveal any particular
association of these asteroids to any specific species
of seagrass nor percentage area coverage of sea-
grass as they were observed throughout the seagrass
area. In terms of canopy heights of seagrass and
abundance of asteroids, areas with lower canopy
heights (in particular from the genera Halodule ,
Cymodocea and Halophila) have higher abundance
in composition of asteroids compared to areas
dominated by high canopy of seagrass ( Enhalus
acroides ) no asteroids where observed.
Vonk et al. (2010) proposed that macrobenthic
organisms including P. nodosus generally prefer
area with high seagrass biomass due to increased
habitat complexity and shelter from predation.
Scheibling (1980) and Scheibling & Metaxes
(2008) found that Oreaster reticulatus and Pro-
toreaster nodosus on seagrass bed feed on microbial
and microalgal films, detritus on the surface of sea-
grass and macroalgae. Scheibling & Metaxes
(2008) also noted the presence of detritus mainly
made out of decomposing seagrass blades and also
epiphytes on the seagrass in the stomach contents
of P nodosus in Palau. Some sea stars also utilize
the seagrass as a transition habitat in juvenile period
as exhibited by A. typicus (Bos et al., 2011), where
the juveniles migrate from mangrove to sandy and
seagrass areas before proceeding to shores. This in-
dicates that seagrass beds are important habitats that
are closely linked to asteroids.
The present study suggests the association of
asteroids to sea grass habiat. There are many other
seagrass beds in the Peninsular Malaysia, yet to be
surveyed, that possibly harbor other species of sea
stars. Future studies in this region should be done
to reveal new records of species and to fill in the
gap of species list as well as geographical distribu-
tion of sea stars.
Figure 8. Dorsal view of Protoreaster nodosus.
Figure 3. Field photograph of Luidia maculata.
ACKNOWLEDGEMENTS
We are especially grateful to members of the
Marine Science Lab, Universiti Sains Malaysia and
Dr. Yuji Ise from University of Tokyo for their kind
assistance during the field and laboratory work. We
also want to mention the contribution from Univer-
sity Putra Malaysia for sampling and logistic ar-
rangements. This study was in collaboration with
the Japan Society for the Promotion of Science for
the Asian CORE Program (Coastal Marine Science
in Southeast Asia: COMSEA). We are also grateful
for the financial support from the Ministry of
458
Woo Sau Pinn et alii
Higher Education Malaysia (MOHE) provided
through the grant: 304/PB/650630/U137.
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Biodiversity Journal, 2014, 5 (4): 459-470
Contribution to the knowledge of the Cicindelidae of Benin
with collecting notes (Coleoptera Cicindelidae)
Arnost Kudrna 1 & Philippe Le Gall 2,3
1 Faculty of Science, University of South Bohemia, Branisovska 31, CZ-370 05, Ceske Budejovice, Czech Republic
2 IRD, Institut de Recherche pour le Developpement, BP 1857 Yaounde, Cameroon. UR 072
3 Laboratoire Evolution, Genomes et Speciation, UPR, 9034, Centre National de la Recherche Scientifique (CNRS), 91198 Gif, sur
Yvette Cedex, France et Universite Paris-Sud 11, 91405 Orsay, Cedex, France
^Corresponding author, e-mail: kudmaa@seznam.cz
ABSTRACT A checklist of Coleoptera Cicindelidae presently known from Benin is given. Nine taxa are
recorded for the first time from this country. Collecting data, habitat and behaviour observations
of adults made by the first author during two expeditions are given along with collecting data
provided by the second author.
KEY WORDS Cicindelidae; new records; collecting notes; West Africa; Benin.
Received 18.09.2014; accepted 05.11.2014; printed 30.12.2014
INTRODUCTION
Benin is a small country (about 700 km long and
from 120 to 200 km wide) bordering Togo in the
west, Nigeria in the east and Niger and Burkina
Faso in the north. Benin has several rivers, in
particular two of them that are restricted to the
country: the Oueme River going throughout a large
part of the territory from the north to the south and
the Mono. Semi-deciduous forests probably cov-
ered the southern part of Benin in the past, however
long presence of humans in these areas resulted in
extensive deforestation. Nevertheless, still remain
few small patches of forests, such as Niaouli and
Pobe which are of particular interest. At present the
central part of Benin is largely covered by Guinean
savannas, as result of deforestation. The north part
of Benin is composed of Guineo-sudanian and
sudanian savannas.
The country is situated in a very special eco-
logical area known as the Dahomey-gap (Dahomey
was the former name of Benin). Dahomey gap is
generally considered as an area where the savannas
descend to the Atlantic coast and where forests are
completely absent. This area displays a high biodi-
versity of insects. The high biodiversity and the
relatively a few published data treating Cicindelidae
from Benin motivated our research and this paper.
MATERIAL AND METHODS
Taxonomic classification used here follows the
last complex work on Cicindelidae of Africa (Wer-
ner, 2000a; 2000b) and the only work exclusively
studying Cicindelidae of Benin (Cassola, 2007).
Most of the data and observations resulted from the
first author's two collecting expeditions and the
additional valuable informations came from long-
term residence of the second author.
All specimens considered in this study are in the
first author's collection except for specimens with
abbreviation PLC belonging to the collection of the
second author.
460
Arnost Kudrna & Philippe Le Gall
RESULTS
List of species presently known from Benin
Family Cicindelidae Latreille, 1806
Subfamily Cicindelinae Csiki, 1906
Tribus Megacephalini Csiki, 1906
Subtribus Megacephalina W. Horn, 1910
Genus Megacephala Latreille, 1802
M. (M) quadrisignata quadrisignata Dejean,
1829
M. (M.) quadrisignata rivalieri Basilewsky,
1966
M. (M) bocandei bocandei Guerin, 1848
M. (M) denticollis schultzeorum W. Horn, 1904
M. (M) megacephala (Olivier, 1790) new coun-
try record
Tribus Cicindelini Sloane, 1906
Subtribus Prothymina W. Horn, 1910
Genus Prothyma Hope, 1838
P. (P.) concinna concinna (Dejean, 1831) new
countiy record
P. (P) concinna anosignata Bates, 1878
P. (P) leprieuri leprieuri (Dejean, 1831) new
country record
Genus Euryarthron Guerin, 1 849
E. dromicarium (Kolbe, 1 894) new countiy record
E. walterhorni Cassola, 1983 new country record
E. saginatum (W. Horn, 1912)
E. gibbosum (W. Horn, 1894)
E. planatoflavum (W. Horn, 1 922) new country
record
Subtribus Cicindelina W. Horn, 1908
Genus Elliptica Fairmaire, 1884
E. lugubris (Dejean, 1825)
E. longestriata longestriata (W. Horn, 1912)
Genus Ropaloteres Guerin, 1 849
R. vittatus (Fabricius, 1801)
R. congoensis congoensis (Fleutiaux, 1893)
R. feisthamelii (Guerin, 1 849) new country re-
cord
R. nysa nysa (Guerin, 1 849)
R. cinctus (Olivier, 1790)
Genus Hipparidium Jeannel, 1946
H. interruptum (Fabricius, 1775)
Genus Calochroa Hope, 1838
C. flavomaculata sexsignata (Mandl, 1954) new
country record
Genus Calomera Motschulsky, 1862
C. fimbriata fimbriata (Dejean, 1831)
Genus Lophyra Motschulsky, 1859
Subgenus Lophyra Motschulsky, 1859
L. neglecta neglecta (Dejean, 1825)
L. senegalensis (Dejean, 1825)
Subgenus Stenolophyra Rivalier, 1958
L. (S'.) luxerii (Dejean, 1831)
L. (S'.) saraliensis saraliesis (Guerin, 1849)
Genus Habrodera Motschulsky, 1862
H. nilotica nilotica (Dejean, 1825)
H. nitidula nitidula (Dejean, 1825)
Genus Chaetodera Jeannel, 1946
Ch. regalis regalis (Dejean, 1831)
Genus Cylindera Westwood, 1831
Subgenus Ifasina Jeannel, 1946
C. (/.) lutaria (Guerin, 1849) new country record
C. (/.) decellei Basilewsky, 1968
C. (/.) octoguttata octoguttata (Fabricius, 1787)
Genus Myriochila Motschulsky, 1862
Subgenus Myriochila Motschulsky, 1862
M. peringueyi peringueyi (W. Horn, 1895)
M. plurinotata (Audoin et Brulle, 1839)
M. melancholica melancholica (Fabricius, 1798)
Subgenus Monelica Rivalier, 1950
M. (M) flavidens flavidens (Guerin, 1849)
M. (M) vicina vicina (Dejean, 1831)
M. (M) dumolinii (Dejean, 1831)
M. (M) legalli Kudrna, 2008
Genus Cratohaerea Chaudoir, 1850
C. chrysopyga (W. Horn, 1 892)
Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)
461
Species with listed examined material col-
lected by both authors supplemented with re-
marks (if available)
Genus Megacephala Latreille, 1802
Megacephala quadrisignata quadrisignata
Dejean, 1829
Examined material. N. Benin, Kosso, V.1996,
several specimens in PLC; Tanguieta V- VI. 1998,
several specimens in PLC; Nanebou, VII.2001,
several specimens in PLC; C. Benin, Ekpa V.1996,
5 males, 4 females in PLC.
Megacephala quadrisignata rivalieri Basilewsky,
1966
Examined material. N. Benin, Kosso, 1 male
in PLC; Benin, Nanebou, 1 male in PLC; Benin,
Serou (Djougou), 1 female in PLC.
Megacephala bocandei Guerin, 1848 (Pig. 1)
Examined material. NE Benin, E of Kandi, 4
km W of Bensekou, 24-25.VI.2001, A. Kudma jr.
legit, 1 male; NW Benin, 15 km N of Kouarfa,
Bouyagnindi village, 27-28.VI.2001, A. Kudrna jr.
legit, 1 female.
Remarks. The cited pair are the only specimens
of M. bocandei captured during both first author's
trips. The male run quickly in night on black soil
path, just where the path left grassy area reach in
trees and entered in the field. The female was
observed in the late morning of a sunny day in
wooded area with high grass and neighbouring
field, moving quickly, probably searching for a prey.
Megacephala denticollis schultzeorum W.
Horn, 1904 (Pig. 2)
Examined material. Benin, village Akongbere,
near Save, 19-26.IV.2000, A. Kudrna jr. legit, 2
males, 2 females; Kosso : V-VI. 1997- 1999, numer-
ous specimens in PLC; Serou, V-VI. 1997- 1999, nu-
merous specimens in PLC; Guinlerou, 15 km west
of Parakou, IV- VII. 1996- 1998, numerous speci-
mens in PLC.
Remarks. Specimens were found in night stand-
ing on dark paths through dense woodland area with
high grass. One female came to light. A torso of a
dead adult was found at the same locality in June
2001 .
Megacephala megacephala (Olivier, 1790)
Examined material. NE Benin, E of Kandi,
around Saa, 21-23.VI.2001, A. Kudrna jr. legit, 1
male, 4 female.
Remarks. According to Basilewsky (1966), this
species is widespread from Senegal and Mauritania
to Chad and occurs in sahelian zone or neighbour-
ing areas only. The cited population here reported
was discovered in northern area of Benin, where
the countryside seems to be more dry and hotter.
Specimens were captured during night on sandy
roads and occasionally came to light. One speci-
men was found quickly running through grasses in
the end of about two hours lasting hard storm
accompanied with intensive rain. New country
record.
Genus Prothyma Hope, 1838
Prothyma concinna concinna (Dejean, 1831)
Examined material. NE Benin, E of Kandi, 7
km E of Bensekou, 23-24. VI. 2001, A. Kudma jr.
legit, 2 males.
Remarks. The first author observed four adults,
but managed to catch only two of them due to their
very rapid movement from small bare places where
discovered, into grass or other hiding-places. These
adults didn't fly. New country record.
Prothyma concinna anosignata Bates, 1878
Examined material. S Benin, Niaouli,
20.X. 1996, 1 female in PLC; S Benin, Niaouli, 10.
VII. 2002, 1 male in PLC; 1 female; S Benin,
Niaouli, 20. XI. 2003, 1 female in PLC; Benin,
Attogon, V.2001, 1 female in PLC; N Benin,
Tanguieta, 20.VII.1998, 1 female in PLC; Benin,
Penessoulou, VI. 1997, 1 male in PLC.
Prothyma leprieuri leprieuri (Dejean, 1831)
Examined material. Penessoulou, 55 km S
Djougou, Atakora Benin, Loko/P.Le Gall
Remarks. A single female specimen without
date record, collected by the second author most
probably at the light. The discovery of this species
462
Arnost Kudrna & Philippe Le Gall
Figure 1. Megacephala ( Megacephala ) bocandei, E of Kandi, 21.3 mm
Figure 2. Megacephala ( Megacephala ) denticollis schultzeorum, near Save, 31.5 mm
in Benin is not surprising due to its wide distribu-
tion from Senegal to Ethiopia. New country record.
Genus Euryarthron Guerin, 1 849
Euryarthron dromicarium (Kolbe, 1894) (Fig. 3)
Examined material. Benin, Bembereke, 2 km
W of Gando, 02-03.VII.2001, A. Kudrna jr. legit, 1
female; NW Benin, 5 km N of Tanguieta, direction
Tanougou, 28-29.VI.2001, A. Kudrna jr. legit, 3
males.
Remarks. A very beautiful wingless species of
Euryarthron which is extremely difficult to find in
Benin. It seems, that this species prefers meadows
or grassy places at the edges of forested areas.
Adults were discovered on bare places, trying to
escape into the grass, when disturbed. One male
specimen came to light. New country record.
Euryarthron walterhorni Cassola, 1983
Examined material. Benin, Tanguieta,
10.V.1997, 1 female; Kosso, VI. 1998, 2 males, 2
females; Benin, Serou VI.2000, 1 male, 1 female;
Benin, Serou, VII. 1998, 1 female. All specimens in
PLC.
Remarks. New country record.
Euryarthron saginatum (W. Horn, 1912) (Fig. 4)
Examined material. NE Benin, E of Kandi, 4
km W of Bensekou, 24-25.VI.2001, A. Kudrna jr.
legit, 2 females; NE Benin, E of Kandi, around Saa,
21-23.VI.2001, A. Kudrna jr. legit, numerous spec-
imens.
Remarks. This species was found on white-
grey soil road through dry woodland with lot of aca-
cia trees. When discovered, it tried to escape flying
Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)
463
Figure 3. Euryarthron dromicarium, S ofKerou, 13 mm
Figure 4. Euryarthron saginatum, E of Kandi, 13.3 mm
away and sit down into the nearby grass. On this
road it lived together with Myriochila plurinotata
and M. ( Monelica ) vicina vicina. In another occa-
sion it was also found in sparse acacia wood.
Euryarthron gibbosum (W. Horn, 1894)
Examined material. Benin, village Alcongbere,
near Save, 19.IV-26.IV.2000, A. Kudma jr. legit, 6
males, 3 females; NE Benin, E of Kandi, 4 km W
of Bensekou, 24-25. VI. 2001, A. Kudma jr. legit, 2
males; NE Benin, E of Kandi, 7 km E of Bensekou,
23-24.VI.2001, A. Kudma jr. legit, 1 male; NW
Benin, 5 km N of Tanguieta, direction Tanougou,
28-29.VI.2001, A. Kudma jr. legit, 1 female.
Remarks. In May 2000 this species appeared
suddenly in the dense woodland area around
Alcongbere village, near Save. Whilst first week of
intensive collecting there was unproductive, during
four next days about 15 adults, at the same, for-
merly empty places, were caught. Few more speci-
mens were found in northern parts of country. This
species prefers shaded places with sparse grass,
paths or roads inside woods.
Euryarthron planatoflavum (W. Horn, 1922)
Examined material. Penessoulou IV. 1998, 1
male in PLC.
Remarks. New country record.
Genus Elliptica Fairmaire, 1884
Elliptica lugubris (Dejean, 1825)
Examined material. NE Benin, E of Kandi, 4
km W of Bensekou, 24-25. VI.2001, A. Kudrna jr.
legit, 1 male; N Benin, S of Kerou, 7 km W
Yakrigourou, 25-26. VI. 2001, A. Kudrna jr. legit, 2
464
Arnost Kudrna & Philippe Le Gall
females; NW Benin, 5 km N of Tanguieta, direc-
tion Tanougou, 28-29.VI.2001, A. Kudrna jr. legit
3 females, 1 male; NW Benin, 15 kmN ofKouarfa,
Bouyagnindi village, 27-28.VI.2001, A. Kudrna jr.
legit, 4 males, 3 females; NE Benin, E of Kandi, 7
km E of Bensekou, 23-24. VE2001, A. Kudrna jr.
legit, 1 male; Benin, Bemberelce, 7 km W of
Gando, 03 -04. VII. 2001, A.Kudrna jr. legit, 2
males; Benin, Bembereke, 2 km W of Gando, 02-
03. VII. 2001, A. Kudrna jr. legit, 1 male; Penes-
soulou, VI.1998-VI.1999, numerous specimens in
PLC; Serou.
Remarks. This very beautiful large species was
present at most of the localities, but usually in few
specimens only. Horn (1915) described subspecies
E. lugubris anthrax, based on the black coloura-
tion. However, the black specimens represent
merely a variation without any taxonomic value.
Interesting is the proportion between this black
form and the common black-yellow specimens:
first author observed only one anthrax variation
along tens of individuals on all of the collecting
spots except locality 5 km N of Tanguieta, where
six from eight caught specimens were black. This
locality, near Atacora Mountains with very sparse
wood with dominance of acacia trees was very hot
and dry place. Elliptica lugubris is generally
silvicolous dwelling species preferring shaded
grassy places.
Elliptica longestriata longestriata (W. Horn, 1912)
Examined material. NW Benin, N of Natitin-
gou, 5 kmNE ofKouarfa, 26-27.VI.2001, A. Ku-
drna jr. legit, 1 female, 1 male; NE Benin, E of
Kandi, 4 km W of Bensekou, 24-25. VI. 2001, A.
Kudrna jr. legit, 1 male, 1 female; NW Benin, 30
km SE of Natitingou, 5 km E of Sina Issire,
30.VI-01.VII.2001, A. Kudrna jr. legit, 2 females;
NW Benin, 15 km N of Kouarfa, Bouyagnindi
village, 27-28. VI. 2001, A. Kudrna jr. legit, 1
male.
Remarks. A very surprising discovery of the
species in Benin, as it was in the time of collecting
known from north of former Zaire and Central
African Republic only. This indicates a much
wider distribution than supposed. Adults were
found always on dark soil with sparse grass,
usually on the edges of fields or directly inside
when uncultivated.
Genus Ropaloteres Guerin, 1849
Ropaloteres vittatus (Fabricius, 1801)
Examined material. NW Benin, 30 km SE
Natitingou, 5 km E of Sina Issire, 30.VI-
01.VII.2001, A. Kudrna jr. legit, 1 female; Benin,
village Akongbere, near Save, 19-26.IV.2000, A.
Kudma jr. legit, 6 males, 3 females.
Remarks. R. vittatus was very rare to find in
Benin during both expeditions. Only few specimens
on very few localities were discovered. It prefers
dark soil paths and clearings in shaded woodland
areas.
Ropaloteres congoensis congoensis (Fleutiaux,
1893)
Examined material. NW Benin, N of Natitin-
gou, 5 kmNE ofKouarfa, 26-27.VI.2001, A. Ku-
drna jr. legit, 7 females, 4 males; NW Benin, 30
km SE Natitingou, 5 km E of Sina Issire, 30.VI-
01. VII. 2001, A. Kudrna jr. legit, 2 males, 2 fe-
males; N. Benin, Ekpa, VI. 1996, 2 males, 1 female
in PLC.
Remarks. This beautiful species was found on
the three cited localities only. On one occasion four
specimens were collected on the edge of a sandy
road and nearby meadow, another time it was
discovered on red soil with turfs of high grass.
Adults were usually a little bit lazy to fly and
preferred rapid run into the shadow of the turfs.
Only when disturbed repeatedly, they flew a few
meters and sat down again near to turfs. After
settling they often disappeared by running through
grasses somewhere on the reverse side, and there-
fore they were hardly found again. This beetle
seems to be generally very rare, however, when a
spot with its occurrence is found, it is usually pos-
sible to collect numerous specimens.
Ropaloteres feisthamelii (Guerin, 1849)
Examined material. NW Benin, 30 km SE
Natitingou, 5 km E of Sina Issire, 30. VI-
01.VII.2001, A. Kudrna jr. legit, 1 female; NW
Benin, N of Natitingou, 5 km NE ofKouarfa, 26-
27.VI.2001, A. Kudma jr. legit, 1 female; N Benin,
S of Kerou, 7 km W Yakrigourou, 25-26.VI.2001,
A. Kudrna jr. legit, 1 female, 2 males; NW Benin,
15 km N of Kouarfa, Bouyagnindi village, 27-
Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)
465
28.VI.2001, A. Kudrna jr. legit, 1 male; NW
Benin, 5 km N of Tanguieta, direction Tanougou,
28-29.VI.2001, A. Kudrna jr. legit, 1 male; Benin,
Bembereke, 7 km W of Gando, 03-04.VII.2001,
A. Kudrna jr. legit, 1 male, 1 female; Serou, V.
2000, 1 female in PLC.
Remarks. Relatively common species occurring
in grassy places in woodland areas, regularly at-
tracted to light. New country record.
Ropaloteres nysa nysa (Guerin, 1849)
Examined material. Benin, village Alcongbere,
near Save, 19.IV-26.IV.2000, A. Kudrna jr. legit,
numerous specimens; NW Benin, 15 1cm N of
Kouarfa, Bouyagnindi village, 27-28. VI.2001, A.
Kudrna jr. legit, 1 male, 2 females; NE Benin, E of
Kandi, 7 km E of Bensekou, 23-24. VL2001, A.
Kudrna jr. legit, 1 male; NW Benin, 5 km N of
Tanguieta, direction Tanougou, 28-29.VI.2001, A.
Kudrna jr. legit, 3 males, 1 female; Benin, Bembe-
reke, 2 km W of Gando, 02-03.VII.2001, A. Ku-
drna jr. legit, 1 male, 1 female; Penessoulou,
V-VI. 1999-2000, numerous specimens in PLC.
Remarks. Very common species with the
same habitat and behaviour as the previous R.
feisthamelii , often coming to light.
Ropaloteres cinctus (Olivier, 1790)
Examined material. Benin, village Alcongbere,
near Save, 19.IV-26.IV.2000, A. Kudrna jr. legit
numerous specimens; NE Benin, E of Kandi, 4 km
W of Bensekou, 14-25.VI.2001, A. Kudmajr. legit,
2 males, 2 females; N Benin, S of Kerou, 7 km W
Yakrigourou, 25-26. VL2001, A. Kudmajr. legit,
numerous specimens; NW Benin, 15 km N of
Kouarfa, Bouyagnindi village, 27-28.VI.2001, A.
Kudmajr. legit, 2 males, 1 female; NE Benin, E of
Kandi, 7 km E of Bensekou, 23-24. VI. 2001, A. Ku-
dmajr. legit, 2 males, 1 female; Benin, Bembereke,
2 km W of Gando, 02-03 .VII. 2001, A. Kudmajr.
legit, numerous specimens.
Remarks. Probably the commonest species of
those, which prefer grassy, shadowed places in
woodlands. This species, in contrast to Elliptica
lugubris, occurred only on a few of the visited
localities, but there it was abundant.
Genus Hipparidium Jeannel, 1946
Hipparidium interruptum (Fabricius, 1775)
Examined material. Benin, near Cove, E of
Abomey, 16.IV.2000, A. Kudmajr. legit, 1 female;
Pobe, Aguigadji, V.1998, 1 female in PLC.
Remarks. Female from E of Abomey was found
on shaded dark soil path inside palm plantation.
Genus Calochroa Hope, 1838
Calochroa flavomaculata sexsignata (Mandl, 1954)
Examined material. Africa/Benin, W-Nat.
Park, X.2002, Mekrou river, Triple Point, 1 male;
Benin, Penessoulou, 12.XI.2000, at light, 1 male, 1
female in PLC.
Remarks. New country record.
Genus Calomera Motschulsky, 1862
Calomera fimbriata fimbriata (Dejean, 1831)
Examined material. Benin, Banks of river
Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.
Kudrna jr. legit, numerous specimens; Benin,
Cove: 20. VI. 2000, numerous specimens in PLC;
Benin, Cove: 27. VI. 2000, numerous specimens in
PLC; Benin, Cove: 5. VI. 2001, numerous speci-
mens in PLC.
Remarks. Adults of this species were present in
huge masses on yellowish sand around river
Oueme, where also Lophyra neglecta neglecta, L.
senegalensis, Cylindera ( Ifasina ) octoguttata oc-
toguttata and Habrodera nilotica nilotica occurred.
Occasionally, beautiful blueish specimens (in
proportion about 1 : 1 00) were caught.
Genus Lophyra Motschulsky, 1859
Subgenus Lophyra s.str.
Lophyra {Lophyra) neglecta neglecta (Dejean,
1825)
Examined material. Benin, Banks of river
Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.
Kudrna jr. legit, numerous specimens; Benin,
Cove, VI.2000, numerous specimens in PLC;
Toffo, IIII.2001, numerous specimens in PLC.
466
Arnost Kudrna & Philippe Le Gall
Figure 5. Cylindera ( Ifasina ) lutaria, W of Gando, 7.8 mm
Figure 6. Myriochila ( Myriochila ) peringueyi, Ndali, 10.1 mm
Remarks. Very common species found on sand
or sandy road near water.
Lophyra {Lophyra) senegalensis (Dejean, 1825)
Examined material. Benin, banks of river
Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.
Kudrna jr. legit, numerous specimens; Benin, vil-
lage Akongbere, near Save, 19-26.IV.2000, A. Ku-
dma jr. legit, numerous specimens; NE Benin, E of
Kandi, 7 1cm E of Bensekou, 23-24. VI. 2001, A.
Kudrna jr. legit, 1 male, 1 female.
Remarks. This species does obviously not
prefer places near water, but was found on many
localities on sandy roads. Even on the river banks
it lives further to water. A common species in
Benin.
Subgenus Stenolophyra Rivalier, 1958
Lophyra ( Stenolophyra ) luxerii (Dejean, 1831)
Examined material. Benin, village Akongbere,
near Save, 19.IV-26.IV.2000, A. Kudrna jr. legit,
numerous specimens; NW Benin, 15 km N of
Kouarfa, Bouyagnindi village, 27-28. VI. 2001, A.
Kudma jr. legit, 1 male, 1 female; NE Benin, E of
Kandi, 7 1cm E of Bensekou, 23-24.VI.2001, A. Ku-
drna jr. legit, numerous specimens; Benin, Niaouli,
VI. 1997-2002, numerous specimens inPLC; Serou,
VI. 1999, 11 males, 12 females in PLC.
Remarks. Occurs in woodland areas and
prefers dark soil roads and paths. A relatively
common species.
Genus Habrodera Motschulsky, 1862
Habrodera nilotica nilotica (Dejean, 1825)
Examined material. Benin, banks of river
Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)
467
Figure 7. Myriochila ( Monelica ) vicina, N of Natitingou, 9.2 mm
Figure 8. Myriochila ( Monelica ) legalli, N of Natitingou, 9.75 mm
Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.
Kudmajr. legit, numerous specimens.
Remarks. This species was found on yellowish
sand of river banks.
Habrodera nitidula nitidula (Dejean, 1825)
Examined material. Benin south, Grand-Popo,
ocean coast, 17.04.2000, A. Kudmajr. legit, 14
males, 2 females.
Remarks. A seashore species. The specimens
were caught on a huge long sandy beach under
windy conditions, always in a large distance from
a water line. Uncommon on this beach.
Genus Cylinder a westwood, 1831
Subgenus Ifasin a Jeannel, 1946
Cylindera ( Ifasina ) lutaria (Guerin, 1849) (Fig. 5)
Examined material. NE Benin, E of Kandi, 4
km W ofBensekou, 24-25. VI. 2001, A. Kudmajr.
legit, 1 female; NE Benin, E of Kandi, 7 km E of
Bensekou, 23-24. VI. 2001, A. Kudmajr. legit, 7
males, 1 female; Benin, Bembereke, 7 km W of
Gando, 03-04. VII. 2001, A. Kudrna jr. legit, 1
male, 1 female; Benin, Bembereke, 2 km W of
Gando, 02 -03. VII. 2001, A. Kudmajr. legit, 2
males.
Remarks. C. (/.) lutaria was found on various
localities, but always near puddles or in muddy or
moist places, usually in few specimens only. A rare
species in Benin. New record for this country.
Cylindera {Ifasina) octoguttata octoguttata
(Fabricius, 1787)
Examined material. Benin, banks of river
Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.
468
Arnost Kudrna & Philippe Le Gall
Kudma jr. legit, numerous specimens; NE Benin, E
of Kandi, 7 km E of Bensekou, 23-24.VI.2001, A.
Kudma jr. legit, 1 male.
Remarks. This very common species was
present in swarms around puddles just next to river.
On several occasions it was captured near brooks
and small rivers.
Genus Myriochila Motschulsky, 1862
Subgenus Myriochila Motschulsky, 1862
Myriochila {M.) peringueyi peringueyi (W.
Horn, 1895) (Fig. 6)
Examined material. Benin, village Akong-
bere, near Save, 19.IV.-26.IV.2000, A. Kudma jr.
legit, 1 female; Benin, Ndali, 3 km W of Sontou,
04-05. VIE2001, A. Kudrna jr. legit, numerous
specimens.
Remarks. The species was abundant west of
Sontou inside a forest area on a flat volcanic rock,
partly covered with a thin layer of dark soil. No
water was present in the vicinity. This species with
unusual red-green body reflexions seems to prefer
rocks or stony places, as also the only female
collected near village Akongbere was discovered in
slightly muddy situation on dark soil road, just
where the road cross a big flat rock.
Myriochila (M.) plurinotata (Audoin et Brulle,
1839)
Examined material. NE Benin, E of Kandi, 7
km E of Bensekou, 23-24. VE2001, A. Kudrna jr.
legit, numerous specimens; NW Benin, 5 km N of
Tanguieta, direction Tanougou, 28-29.VI.2001, A.
Kudma jr. legit, numerous specimens; NW Benin,
N of Natitingou, 5 km NE of Kouarfa, 26-
27.VE2001, A. Kudrna jr. legit, numerous speci-
mens; NW Benin, 15 km N of Kouarfa,
Bouyagnindi village, 27-28.VI.2001, A. Kudma jr.
legit, 2 males, 3 females.
Remarks. This species was present on several
localities, usually sitting on soil roads or other bare
places in sunny situation. On the locality situated 5
km NE of Kouarfa it occured together with another
nine species: Elliptica lugubris, E. longestriata
longestriata, Myriochila ( Monelica ) dumolinii, M.
(M.) vicina, M. (M.) legalli, Lophyra ( Stenolo -
phyra ) luxerii, Ropaloteres cintus, R. congoensis
congoensis, R. feisthamelii. Regularly came to light.
Not rare in Benin.
Myriochila (M.) melancholica melancholica
(Fabricius, 1798)
Examined material. Benin, banks of river
Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.
Kudma jr. legit, numerous specimens; Benin,
village Akongbere, near Save, 19.IV-26.IV.2000, A.
Kudma jr. legit, numerous specimens; Toffo, 12.11.
2001, several specimens in PLC; Serou, VI. 1998,
several specimens in PLC.
Remarks. This very common species was
present at most of the collecting places always near
water.
Subgenus Monelica Rivalier, 1950
Myriochila ( Monelica ) flavidens flavidens
(Guerin, 1849)
Examined material. NE Benin, E of Kandi,
around Saa, 2 1-23. VI. 2001, A. Kudrna jr. legit,
numerous specimens; NE Benin, E of Kandi, 7 km
E of Bensekou, 23-24.VI.2001, A. Kudma jr. legit,
numerous specimens; Benin, Bembereke, 7 km W
of Gando, 03-04.VII.2001, A. Kudrna jr. legit, 2
males, 3 females.
Remarks. Although considered to be a very rare
species (Werner, 2000), it was observed on many
localities in northern parts of Benin. Adults were
present in masses on laterite soils, always in muddy
or moist places or near puddles, and surely repre-
sented one of the commonest species during the
second collecting trip of the first author.
Myriochila (Monelica) vicina vicina (Dejean,
1831) (Fig. 7)
Examined material. NW Benin, 5 km N of
Tanguieta, direction Tanougou, 28-29. VI.2001, A.
Kudma jr. legit, numerous specimens; N Benin, S
of Kerou, 7 km W Yakrigourou, 25-26. VI.2001, A.
Kudma jr. legit, numerous specimens; NE Benin, E
of Kandi, 7 km E of Bensekou, 23-24. VI.2001, A.
Kudma jr. legit, numerous specimens; NW Benin,
15 km N of Kouarfa, Bouyagnindi village, 27-
28.VI.2001, A. Kudma jr. legit, 1 male, 2 females;
Penessoulou, V.1998 numerous specimens in PLC;
Penessoulou, V.1999 numerous specimens in PLC.
Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)
469
Remarks. During second collecting trip of the
first author, this species was abundantly found in
the northern parts of the country. Specimens were
collected on bare places, paths or roads through
grass or fields.
Myriochila ( Monelica ) dumolinii (Dejean, 1831)
Examined material. Benin, Bembereke, 7 km
W of Gando, 03-04.VII.2001, A. Kudmajr. legit, 2
males; N Benin, S of Kerou, 7 km W Yakrigourou,
A. Kudma jr. legit, 2 females; NW Benin, N of
Natitingou, 5 km NE of Kouarfa, 26-27.VI.2001,
A. Kudrna jr. legit, 1 male ; NW Benin, 30 km SE
Natitingou, 5 km E of Sina Issire, 30. VI-
01.VIE2001, A. Kudmajr. legit, 1 female; Serou,
VI. 1997, several specimens in PLC; Serou,
VIE 1998, several specimens in PLC.
Remarks. Adults came regularly to light. Two
specimens were found on laterite soil road in a
sunny day. Uncommon.
Myriochila (Monelica) legalli Kudrna, 2008
(Fig. 8)
Examined material.NW Benin, N of Natitin-
gou, 5 km NE of Kouarfa, 26-27. VI.2001, A. Ku-
dma jr. legit, 5 males, 2 females; NE Benin, E of
Kandi, 7 km E Bensekou, 23-24. VL2001, A. Ku-
dmajr. legit, 1 male, 1 female; NW Benin, 15 km
N of Kouarfa, Bouyagnindi village, 27-28. VI.2001,
A. Kudmajr. legit, 1 female; S Benin, vill. Akong-
bere, near Save, 16-20.VI.2001, A. Kudmajr. legit,
1 female.
Remarks. Specimens of this recently described
species (Kudma, 2008) were found during sunny
day on dark soil road through dense wood in
forested area and also on laterite soil of a wide field
road in the agricultural area.
Genus Cvatohaerea Chaudoir, 1850
Cratohaerea chrysopyga (W. Horn, 1892)
Examined material. Benin , village Akongbere,
near Save, 19.IV-26.IV.2000, A. Kudmajr. legit, 15
males, 5 females; NE Benin, E of Kandi, around
Saa, 2 1-23. VI.2001, A. Kudmajr. legit, 3 males, 3
females; Benin, Bembereke, 7 km W of Gando, 03-
04.VII.2001, A. Kudmajr. legit, 2 males, 1 female;
Ouidah, 20.V.1996, 1 female in PLC; Benin, Pobe,
X.2001, 1 male in PLC; Niaouli IV-VI.1996 several
specimens in PLC; Niaouli VI. 1998 several speci-
mens in PLC; Niaouli V-VI.1999 several specimens
in PLC; Benin, Parakou, V.1996, several specimens
in PLC; Benin, Kosso, V-VII. 1998-2000, several
specimens in PLC.
Remarks. All specimens of C. chrysopyga were
found on termitaries. They prefer bigger ones,
situated entirely or at least partly in shaded places
and with more or less preserved structure. When
disturbed, they tried to hide themselves by mnning
constantly on the reverse side of the termitaries and
with care it was even possible to catch them by
hand. When adult successfully escaped from behind
the net, then settled on the opposite side of the
termitaries, in the nearby grass or flew away and
disappeared somewhere in the forest. But after
some time, the beetle was back. It was usually
necessary to visit several termitaries to find one in-
habited. Generally one or two specimens together
were found on one termitarium, but in one occasion
even four were present. Relatively rare in Benin.
DISCUSSION
Werner (2000a, b), in his monographic review
of African tiger beetle fauna listed 1 7 species and
subspecies from Benin. Recently Cassola (2007),
in the only so far existing publication devoted
solely to Cicindelidae of Benin reported 31 taxa
(30 species and one subspecies) from this country.
In this contribution we add another nine species as
new for Benin thus the total number is 41. Most
of the species added in this contribution were
expectable to occur in Benin. We suppose that new
records will follow and the number of tiger beetles
taxa known from this beautiful country can exceed
50 or even 55.
ACKNOWLEDGMENTS
We would like to express our thanks to Dr.
Georg Goergen. Moreover the first author thanks to
all of his companions during the two Benin's trips:
Mrs. Libena Kantnerova and Mr. Frantisek Kantner
(Lipi), Mr. Zdenek Andrs (Cemosin), Mr. Borivoj
Vorisek (Ceske Budejovice), Mr. Jin Halada (Ceske
Budejovice), first author’ s father Amost Kudma sr.
470
Arnost Kudrna & Philippe Le Gall
(Rudofov), driver Wirgile Adingni and Mr. and Mrs.
Ahanhanzo.
REFERENCES
Basilewsky P., 1966. Revision des Megacephala d'
Afrique (Coleoptera Carabidae Cicindelinae), Anna-
les Musee Royal de T Afrique Centrale, Serie IN-°8,
n°152, 1-149.
Cassola R, 2007. Studies of tiger beetles. CLXV. New
data from Benin (Coleoptera: Cicindelidae), Rivista
Piemontese di Storia Naturale, 28: 157-164.
Kudrna A., 2008. Myriochila ( Monelica ) legalli sp. n.
from Benin and Senegal (Coleoptera, Cicindelidae),
Entomologia Africana, 13: 33-37.
Werner K., 2000a. The tiger beetles of Africa (Coleoptera:
Cicindelidae), Volume 1, Taita publishers, 191 pp.
Werner K., 2000b. The tiger beetles of Africa (Coleoptera:
Cicindelidae), Volume 2, Taita publishers, 207 pp.
Biodiversity Journal, 2014, 5 (4): 471-474
The first record of Trigonostigma somphongsi (Meinken, 1 958),
a critically endangered species, in its natural habitat of Thai-
land (Cypriniformes Cyprinidae)
Nidsaraporn Petsut',Nonn Panitvong 2 , Sitthi Kulabtong 3 ,Jirawaeth Petsut 1 & Chirachai Nonpayom 4
'Department of Agricultural Technology, Faculty of Science, Ramkhamhaeng University, Bangkok 10240, Thailand; e-mail:
nidsarapom@ni.ac.th (Nidsaraporn Petsut); e-mail: jira3800@sanook.com (Jirawaeth Petsut)
2 Siamensis Biodiversity Conservation Group, 408/144 Phaholyothin Place Bldg 34FL, Phaholyothin Rd., Phayathai, Bangkok
10400, Thailand; e-mail: npanitvong@gmail.com
fisheries Program, Faculty of Agro-Industrial Technology, Rajamangala University of Technology Tawan-ok Chantaburi Campus
Chantaburi 22210, Thailand; e-mail: kulabtong2011@hotmail.com
4 534/26 Soi Phaholyothin 58 Phaholyothin Rd. Sai Mai, Bangkok, Thailand; e-mail: sornl33@hotmail.com
^Corresponding author
ABSTRACT A population of a critically endangered Trigonostigma somphongsi (Meinken, 1958) has been
discovered in a deepwater rice field, floodplain of Bangpakong Basin, Nakhomnayok Province,
central Thailand. The population was the first record of this species in its natural habitat since
its description by Meinken in 1958. The species appeared to be a seasonal horizontal migration
species, since it migrates to breed in the floodplain during the rainy season between July and
November and migrates back into the main channel during the dry season.
KEY WORDS Trigonostigma somphongsi ; Cyprinidae; Bangpakong; Thailand.
Received 19.09.2014; accepted 12.11.2014; printed 30.12.2014
INTRODUCTION
Trigonostigma somphongsi (Meinken, 1958)
was placed in the genus Rasbora (Bleeker, 1859)
(Meinken, 1958) and, subsequently, in the genus
Trigonostigma Kottelat et Witte, 1999 described by
Kottelat & Witte (1999).
The genus Trigonostigma is a well defined
group comprising 4 species: T. heteromorpha
(Duncker, 1904), as type species, with its distribu-
tion in Malay Peninsula, T. espei (Meinken, 1967)
found in south eastern and southern part of Thai-
land, and T. hengeli (Meinken, 1956) reported from
Sumatra; the fourth species, T. somphongsi, differs
from the rest of the genus in its dark pattern which
occurs as a strait horizontal line that extends from
the base of the caudal fin and ends just after it
passed the posterior part of the dorsal fin instead of
showing the wedge-like marking of other species in
the genus.
Apart from external characters of the body
shape and marking, this genus also differs from
other Rasborins in its breeding strategy since
parents deposit eggs under broad leaves of aquatic
plants instead of scattering eggs like most others.
In this regard, it is interesting to note the sex ratio
screwed towards males in this species observed in
this survey.
The type series of T. somphongsi was said to
come from aquarium trade, sent to Meinken by
Somphongs Aquarium, an ornamental fish exporter
run by Mr. Somphongs Lekaree with its base in
472
Nidsaraporn Petsut et alii
Thailand. The fish was thus, named after Somphong
in honor of his contribution of the type series.
No detail of its habitat was given in the paper;
Meinken only mentioned that it was from Southern
Thailand (Meinken, 1958). The fish appeared in
various hobby publishing during the 70s in both
Europe and Asia before completely disappearing for
some 20 years. It wasn’t until 2006 when three T.
somphongsi were found among a batch of Boraras
urophthalmoides (Kottelat, 1991) by Uta Hanel
(Germany). They happened to be one male and two
females thus forming the core for a captive breeding
population which is still going on in Europe, mainly
Germany and England, as well as in Thailand.
However, to date, no fish has ever been ob-
served in its natural habitat, which prompted IUCN
to list it as Critically Endangered (Vidthayanon,
2013) and listed it as world’s 100 most threaten
species (Baillie & Butcher, 2012). Upon our survey
of a flood plain in deepwater rice field, flood plains
of Bangpakong Basin, Nakhornnayok Province,
central Thailand, a population of T. somphongsi was
discovered. Its habitat and population demography
will be described here.
MATERIAL AND METHODS
Surveys were conducted by dragging fine mesh
sein, along marginal area of floodplain as well as
along the road and rice field. We also snorkeled to
observe its habitat and behavior under water. All
other species were released on site as quickly as
possible after identification.
All T. somphongsi (Fig. 1) were kept alive for
further study in captivity. Surveys were conducted
from September 2012 to November 2013. Locals
were interviewed for further information and water
quality parameters were measured with methods by
APHA et al. (2009).
Study area
Trigonostigma somphongsi was found in a
deepwater rice field, in the flood plains of Nakhom-
nayok River, Bangpakong Basin, Nakhornnayok
Province, central Thailand (Fig. 2), one of the main
tributaries of Bangpagong River, which empties
into the Gulf of Thailand. The head water, to the
north, originated in KhaoYai National Park, which
is a part of Dong Phayayen-KhaoYai Forest Com-
plex - UNESCO World Heritage site. The area is
characterized by flat land, with numerous water
ways. Majority of the land has been turned into
agricultural land. The main crop is rice ( Oryza sp.).
Our survey plot was in Pak Phli District, Nakom-
nayok Province.
The fish was found in the rice field and in a
densely vegetated ditch, which was flooded by a
nearby river. The water quality parameters are
shown in Table 1 . It is interesting to note the drop
of the water’s pH from 7.98, when it first enters the
floodplain, to 3.8 1 after a few months of inundation.
The field was planted with a variety of rice called
“Banna 423”, developed by the Rice Department of
Thailand. This variety is said to be able to grow as
fast as 1 0 centimeters in 24 hours and can grow as
long as 5 meters, thus being immune to the flood
and forming a dense under- water jungle.
In the same area, the other fish species were sur-
veyed and reported by Petsut et al. (2013a) and Pet-
sut et al. (2013b). A total of 23 species, 8 families
and 4 orders of freshwater fishes were recorded.
The natural aquatic plants in this area was
reported by Petsut et al. (2012) with Poaceae as
WATER QUALITY
PARAMETERS
RESULT
Water temperture (°C) at 1.00
p.m.
31.0-33.5
Transparency (cm)
80 - bottom soil (tran-
sparent)
Water depth (cm) in flood season
300 - 30
Water pH
3.81-7.98
Soil pH
3.85-4.70
Alkalinity (ml/L as CaCCb)
6.37-47.00
Ammonia (ml/L Nitrogen)
0.042 - 0.450
Nitrite (ml/L Nitrogen)
0.076-0.160
Nitrate (ml/L Nitrogen)
0.461 -0.680
Hardness (ml/L as CaCCb)
35-202
Orthophosphate (ml/L Phospho-
rus)
0.020 - 0.022
Table 1 . Water quality parameters in a deepwater rice
field, flood plain of Bangpakong Basin, central Thailand.
The first record of Trigonostigma somphongsi, an critically endangered species, in Thailand (Cypriniformes Cyprinidae) 473
dominant family. The change of benthic fauna com-
position and ecological structure of plankton com-
munities in theses area was reported by Petsut et al.
(2013c) and Petsut et al. (2013d).
RESULTS
During the dry season, i.e. when water has com-
pletely receded into the river, in the area where we
would have found, later, T. somphongsi during the
flooding, only Boraras urophthalmoides and
Trichopsis vittatus (Cuvier, 1831) were observed.
July represented the first month of inundation.
Many species of fishes were found in the floodplain
in abundance. In this period we only caught one T.
somphongsi gravid female.
From September to November, the peak of flood-
ing period, we caught many semi-adult (probably
young of the year), but failed to find any full grown
adults. We believe that the adults only migrate to
breed and then leave the flood plain, back to the
main channel. T. somphongsi is weakly sexual
dimorphic. Females can be distinguished from
males by larger size, plumper belly and less intense
orange coloration on the body. Twelve semi-adults
grew up to be 7 males and 5 females, such a
screwed sex ratio towards males was also reported
in a captive-bred population, although our sample
size is definitely too smail to be conclusive.
Trigonostigma somphongsi were found in a
mixed school with many other small cyprinids,
especially Rasbora borapetensis Smith, 1934,
Amblypharyngodon chulabhornae Vidthayanon et
Kottelat, 1990 and Boraras urophthalmoides
which often form large schools (Fig. 3), some-
times of more than a hundred specimens. These
fishes were found swimming in margin of the
deepwater rice field and in an area with not so
dense aquatic plants. T. somphongsi were found to
be minority in the school with only a few individ-
uals observed. The school was often led by R.
borapetensis (the strongest swimmer), then fol-
lowed by A. chulabhornae with B. urophthalmoi-
des (smallest species) and T. somphongsi at the tail
of the school.
Sometimes the school could be observed eat-
ing suspended food particles stirred up by re-
searchers from the bottom of the floodplain. At
one point, a small crab accidentally stepped on
Figure 1. The female of T. somphongsi is larger (left), the
male (right) shows more intense colors (in breeding tank).
Figure 2. Habitat of T. somphongsi in a deepwater rice
field, flood plains of Bangpakong Basin, central Thailand.
Figure 3. Trigonostigma somphongsi in its natural habitat can
be found in mixed school with many other small cyprinids.
474
Nidsaraporn Petsut et alii
which attracted many of the fish in the area in-
cluding T. somphongsi to come and eat the fresh
prey. Surveys by sein mostly yielded only one T.
somphongsi , if any, among many other individ-
uals of other species; only once during our survey
three individuals turned up.
DISCUSSION
Given that the other 3 species in the genus live
in peat swamps or lowland streams, it is interesting
to find T. somphongsi living in a large river and
migrating to breed in floodplain during the rainy
season. It is highly possible that the range of this
species once occupied most of the central plain of
Chao Phraya River as well as the floodplain of Mae
Klong River, in the west. However, flood control
and lost of habitat have reduced its distribution to
current area. The species appeared to be naturally
low in density in the study area, however the flood-
plain appears to be large enough to support a
healthy population.
Our study showed that the floodplain formed an
integral part to the live cycle of this rare species, it
is thus recommended that the flooding in this area
should be managed so that both human and fishes
can both benefit from it.
ACKNOWLEDGEMENTS
We are grateful to the Research and Develop-
ment Institute Ramkhamhaeng University for finan-
cial support. We also wish to thank the reviewers
for the invaluable editorial advice. We would like
to thank Mr. Thanachai Pangkhamraeng, Mr. Ji-
rawat Polpermpul, Mr. Zhou Hang, Mr. Koji Ya-
mazaki, and Mr. Pavaphon Supanantananont their
for assistance in the fieldwork.
REFERENCES
APHA, AWWA & WEE, 2009. Standard Methods for the
Examination of Water and Wastewater. 18th ed. USA:
American Public Health Association, Washington
D.C., 83 pp.
Baillie J.E.M. & Butcher E.R., 2012. Priceless or
Worthless ? The world’s most threatened species.
Zoological Society of London, 112 pp.
Kottelat M. & Witte K.E., 1999. Two new species of
Microrasbora from Thailand and Myanmar, with two
new generic names for small southeast Asian cyprinid
fishes (Teleostei: Cyprinidae). Journal of South Asian
Natural History, 4: 49-56.
Meinken H., 1958. Mitteilungen der fischbestim-
mungsstelle des VDA. XXIX. Rasbora somphongsi
eine neue Zwergrasbora. Die Aquarien- und Terrarien
Zeitschrift, 11: 67-69.
Petsut N., Kulabtong S. & Petsut R, 2012. Preliminary
survey of biodiversity of aquatic plants in rice field
ecosystem at Upper Bangpakong Basin. Journal of
Faculty of Animal Science and Agricultural Technol-
ogy Silpakorn University, 3: 1-16.
Petsut N., Kulabtong S. & Petsut R, 2013a. Preliminary
survey of freshwater fishes from acid soil area in
upstream of Bangpakong River, Nakhon Nayok
Province, Thailand. Journal of Biodiversity and En-
vironmental Sciences, 3: 33-36.
Petsut N., Kulabtong S. & Petsut R, 2013b. Two new
records of cyprinid fish (Cypriniformes Cyprinidae)
from Thailand. Biodiversity Journal, 4: 411-414.
Petsut N., Kulabtong S. & Petsut R, 2013c. Change of
benthic fauna composition in deepwater rice field
ecosystem. Veridian e-Journal Silpakorn University,
6: 1010-1024.
Petsut N., Kulabtong S. & Petsut R, 2013d. Ecological
structure of plankton communities in acid soil area:
Case study in deep water ricefield ecosystem. The
6th National conference on algae and plankton,
Chiangmai.
Vidthayanon C., 2013. Trigonostigma somphongsi. In:
IUCN 2014. IUCN Red List of Threatened Species.
Version 2014.2. <www.iucnredlist.org>. Downloaded
on 19 September 2013.
Biodiversity Journal, 2014, 5 (4): 475-480
First record of the Caucasus field mouse Apodemus ponticus
Sviridenko, 1936 (Rodentia Muridae) from Iran
Zeinolabedin Mohammadi'*,Jamshid Darvish 1,2 , Fatemeh Ghorbani 1 & Ehsan Mostafavi 3,4
'Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
2 Rodentology Research Department (RRD), Applied Animal Institute (AAI), Ferdowsi University of Mashhad, Mashhad, Iran
department of Epidemiology, Pasteur Institute of Iran, Tehran, Iran
4 Research Centre for Emerging and Reemerging infectious diseases, Pasteur Institute of Iran, Akanlu, Kabudar Ahang, Hamadan,
Iran
’Corresponding author, e-mail: Mohammadi.zeinal@gmail.com
ABSTRACT This study is the first record of six specimens of Apodemus ponticus Sviridenko, 1936 (Rodentia
Muridae) from the Zagros Mountains, north western Iran. Four external features besides 13
linear measurements of the skull and 14 dental characters were measured. This species was
identified by its extensive and well-marked boundary throat spot. In addition, A. ponticus shows
morphometric characters including head and body length (mean= 90.86±2.54), length of bullae
(mean = 6.34=1=0. 1 1), breadth of bullae (mean = 4.77±0. 12) and dental characters consisting of
maxillary tooth row (mean = 3.85±0.06) and mandibular tooth row (mean = 3.90±0.05) which
are different from the sympatric species A. witherbyi Thomas, 1902. Based on our results, the
distributional range of A. pon ticus extends to oak forests of the Zagros Mountains, west Iran
which is considered to be the easternmost boundary of its range.
KEY WORDS Apodemus ponticus ; sympatric; Zagros Mountains; Iran.
Received 22.09.2014; accepted 18.11.2014; printed 30.12.2014
INTRODUCTION
Caucasus field mouse Apodemus ponticus
Sviridenko, 1936 (Rodentia Muridae) is one of the
most ambiguous members of the genus Apodemus
Kaup, 1829. It was first described from Olginka
Village, northwest Caucasus and supposed to be
endemic to southern Caucasus region (Azerbaijan
and Georgia; Ellerman & Morrison-Scott, 1951;
Musser & Carleton, 2005). Its limit expansion
reaches up to south Russia.
Initially, it had been considered intermediate
hybrid between A. sylvaticus (Linnaeus, 1758) and
A. flavicollis (Melchior, 1834) or included in a
superspecies namely A. flavicollis (Heptner, 1940;
Neithammer, 1978). Vereshchagin (1959) misclas-
sified A. ponticus as a form of A. fulvipectus
(Ognev, 1924). However, subsequent studies in-
dicated that Caucasus field mouse is a separate
species.
Differences between Allozyme-electroforetic
patterns of A. ponticus from A. uralensis (Pallas,
1811) (as A. ciscaucasicus Ognev, 1 924), A. wither-
byi (Thomas, 1902) (as A. fulvipectus) and A. flavi-
collis were described by some authors (Mezhzherin,
1990; Mezhzherin et al., 1992; Lavrenchenlco &
Likhnova, 1995). In addition, some diagnostic
karyological features of A. ponticus were identified
(Kozlovsky et al., 1990; Orlov et al., 1996a, b). The
Caucasus field mouse can be diagnosed from A.
witherbyi by multivariate analysis (Lavrenchenko
& Likhnova, 1995).
476
Zeinolabedin Mohammadi etalii
Although, based on mt DNA cytb gene sequen-
ces, Balakirev et al. (2007) proposed unity between
A. ponticus and A. flavicollis. Suzuki et al. (2008)
clustered it as a sister clade of A. flavicollis based
on trees constructed applying four nuclear and one
mitochondrial genes but with weak support for the
formers.
Until recently five species of wood mice of the
genus Apodemus including the following species:
A. witherbyi, A. uralensis, A. hyrcanicus
Vorontsov, Boyeskorov et Mezhzherin, 1992, A.
flavicollis and A. mystacinus were recorded
(Javidkar et al., 2005; Krystufek & Hutterer, 2006;
Darvish et al., 2010; Darvish et al., 2014) and A.
avicennicus has been described by Darvish et al.
(2006) from Iran.
In this study, the first record of A. ponticus as a
member of murine rodents would be added to the
checklist of rodent fauna of Iran.
MATERIAL AND METHODS
The study was done in Kordestan Province, west
Iran from June 2013 to July 2013, using live-traps
and snack baits (Fig. 1).
Specimens were captured and determined based
on cranial and external morphological features,
using keys including: Mezhzherin et al. (1992) and
Vorontsov et al. (1992). Standard vouchers of spec-
imens (skins, skulls, tissues) were deposited in the
Zoology Museum of Ferdowsi University of
Mashhad (ZMFUM).
Specimens were weighted, sexed and four
external characters were measured; besides, 13
linear measurements of the skull were taken using
a vernier calliper accurate to the nearest 0.05 mm
(Table 1). 14 dental measurements were per-
formed with a measuring microscope to 0.001
mm (Table 1).
Figure 1. Location of the study areas: Zagros Mountains, northwestern Iran.
First records of the Caucasus feld mouse Apodemus ponticus Sviridenko, 1 936 (Rodentia Muridae) from Iran 477
Variables A. ponticus n=6 A. witherbyi n=38
Mean ± SE
Min
Max
Mean ± SE
Min
Max
HBL
89.86±2.54
83
103
90.40il.18
77
103
TL
101.33±1.09
97
104
99.56il.17
78
117
HFL
22.71±0.47
21
24
21.37i0.24
15
24
EL
17.43i0.33
14
21
15.79i0.28
11
26
CBL
24.14i0.34
23.28
25.24
23.31i0.10
21.24
24.72
FL
12.51i0.14
11.94
13.20
12.28i0.05
11.32
12.90
PAL
4.88i0.08
4.58
5.34
4.79i0.05
4.12
5.46
ZYGB
13.18i0.18
12.64
14.02
12.72i0.08
11.40
13.88
RW
4.28i0.082
4.00
4.52
4.43i0.04
3.66
4.84
IOC
4.30i0.07
3.92
4.52
4.33i0.02
4.10
4.66
BCW
11.97i0.11
11.56
12.38
11.70i0.04
11.23
12.32
IBW
11.40i0.13
10.94
11.98
10.98i0.50
10.44
12
RH
6.21i.09
5.72
6.54
5.94i0.04
5.40
6.38
BCBH
9.42i0.15
8.54
9.88
8.93i0.04
8.34
9.46
TBL
6.34i0.11
5.76
6.78
5.91i0.05
5.32
6.82
TBW
4.77i0.12
4.28
5.22
4.40i0.02
4.08
4.76
ML
11.98i0.33
10.82
13.44
11.57i0.07
10.34
12.52
Ml.L
1.86i.05
1.55
2.08
1.85i.01
1.69
1.96
Ml.W
1.17i0.04
0.92
1.27
1.16i.01
1.02
1.26
M2.L
1.15i0.02
1.06
1.21
1.13i.01
1.03
1.20
M2.W
1.10i0.03
0.94
1.17
l.lli.01
1.01
1.22
M3.L
0.87i0.02
0.82
1.04
0.84i0.01
0.76
0.98
M3.W
0.82i0.03
0.63
0.95
0.81i.01
0.67
0.93
M.1L
1.77i0.02
1.63
1.89
1.66i0.01
1.17
1.78
M.1W
1.04i0.03
0.84
1.13
1.03i0.01
0.88
1.12
M.2L
1.18i0.01
1.11
1.25
1.14i0.01
1.04
1.25
M.2W
1.06i0.03
0.89
1.18
1.04i0.01
0.90
1.19
M.3L
0.96i0.03
0.79
1.05
0.97i.01
0.88
1.06
M.3W
0.89i0.07
0.74
0.96
0.89i0.04
0.80
1
MxTR
3.83i0.06
3.54
4.14
3.78i0.01
3.54
3.95
MnTR
3.90i0.05
3.68
4.14
3.76i0.01
3.37
3.94
Table 1. External, cranial and dental measurements (in mm) of A. mystacinus and A. witherbyi from northwest of Iran.
478
Zeinolabedin Mohammadi etalii
ABBREVIATIONS. Abbreviations of charac-
ters are as follows (for descriptions of characters
see Frynta et al., 2001; Javidkar et al., 2005, 2007
and Krystufek & Vohralik, 2009): HBL: head and
body length; TL: tail length; HFL: hind foot length;
EF: ear length; CBF: condylobasal length; FF: fa-
cial length; PAF: palatal length; ZYGB: zygomatic
breadth; RW: rostrum width; IOC: interorbital con-
striction; BCW: braincase width; IBW: interbulla
width; RH: height of rostrum; BCBH: height of
braincase with tympanic bulla; TBF: tympanic
bulla length; TBW: tympanic bulla width; ME:
mandible length; Ml.F: length of first upper molar;
Ml.W: width of first upper molar; M2.F: length of
second upper molar; M2.W: width of second upper
molar; M3.F: length of third upper molar; M3.W:
width of third upper molar;M.lF: length of first
lower molar; M.1W: width of first lower molar;
M.2F: length of second lower molar; M.2W: width
of second lower molar;M.3F: length of third lower
molar; M.3W: width of third lower molar; MxTR:
length of maxillary tooth row; MnTR: length of
mandibular tooth row.
RESULTS
Apodemus ponticus is sympatric and syntopic
with A. witherbyi at 1545 m (a.s. 1.) in the western
slopes of the Zagros Mountains. This species was
identified by its extensive and well-marked bound-
ary throat spot.
The length of sole is more than 2 1 mm. A. pon-
ticus shows morphometric characters including
head and body length (mean= 90.86±2.54), length
of bullae (mean = 6.34±0.11), breadth of bullae
(mean = 4.77±0.12) and dental characters consis-
ting of maxillary tooth row (mean = 3.85±0.06) and
mandibular tooth row (mean = 3.90±0.05) which
are different from the sympatric species A. wither-
byi (Table 1).
DISCUSSION
The Zagros Mountains is a part of the Irano-
Anatolian hotspot, one of the richest biodiversity
and endemicity hotspot regions in the world (Mit-
termeier et al., 2012). Irano- Anatolian hotspot also
encompasses the Ponto-Caspian realm including
the regions between Black and Caspian Sea and
southern coast of Caspian Sea proposed the
refugial area for evolution of some endemic lin-
eages of rodents such as Glis glis (Finnaeus, 1766)
(Naderi et al., 2013) and some insectivores (Dubey
et al., 2007a; Dubey et al., 2007b).
In addition, terrestrial exchange is partially con-
ceivable via some corridors (i.e. Aras River valley;
Missone, 1959) between the region and the Cauca-
sus hotspot where the Caucasus field mice were
supposed to be endemic.
The Caucasus field mice are sympatric with
congener species A. witherbyi and A. mystacinus in
Kordestan province. A. ponticus is syntopic with
A. witherbyi in bushy foothills of the Zagros Moun-
tains in 1545 m (a.s.l.) however; it has not been
collected with A. mystacinus at the same altitude.
So, the Caucasus field mice could pass the Aras
valley and establish the populations in the Zagros
Mountains.
Moreover, the Zagros Mountains are the south-
ernmost boundary of the distributional range of the
species. Finally, the Caucasus field mice from Iran
show lower average in size (i.e. CBF =24.14;
MxTR=3.83) comparing to that of specimens re-
ported from Caucasus (CBF =25.53;MxTR=3.98)
and the minimum of the foot length (21 vs 22.5);
based on measurements published by Vorontsov et
al. (1992).
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Biodiversity Journal, 2014, 5 (4): 481-498
Little effect of ecological factors and symbiotic specificity on
the distribution of Medicago subsect. Intertextae (Urban) Heyn
(Fabales Fabaceae) in the Mediterranean Basin
Meriem Laouar & A'l'ssa Abdelguerfi
Ecole Nationale Superieure Agronomique, Belfort, El Harrach 16200 Alger, Algerie; e-mail: laouar_m@yahoo.fr
■"Corresponding author
ABSTRACT In the Mediterranean region, Medicago granadensis Willd. and M. muricoleptis Tineo (Fabales
Fabaceae) of the Intertextae subsection are rare and present, each one in well defined areas,
whereas the others taxa, in the same subsection, M. ciliaris (L.) All. and M. intertexta (L.)
Mill., are more frequent with large distribution. This kind of geographical distribution is not a
coincidence; certainly different factors are the origin of this distribution. In 125 sites of different
Mediterranean countries, the ecology of the four taxa was studied, 34 trapped strains in one
site of Intertextae rhizobiums were characterized by rep-PCR and some symbiotic tests were
carried out. The results confirm that M. muricoleptis and M. granadensis are endemic in the
north and east of the Mediterranean, respectively; whereas, M. ciliaris and M. intertexta are
widespread. Although their geographic specificity, the four taxa showed no important differ-
ences in ecological conditions. M. muricoleptis, given its presence in the north of the Mediter-
ranean only, is distinguished by its precipitation requirement. By inference, the absence of M.
muricoleptis and M. granadensis in some regions is not due to the absence of the symbiont.
We confirm the symbiotic specificity of Sinorhizobium medicae (Rome, 1996) for the
Intertextae subsection and the existence of coevolution between taxa (widespread and endemic)
and rhizobia. We suppose that endemic taxa are in the process of allopatric speciation, which
explains their narrow distribution in the Mediterranean Basin.
KEY WORDS Distribution; diversity; ecology; Intertextae', Medicago', Mediterranean; symbiosis.
Received 15.10.2014; accepted 18.11.2014; printed 30.12.2014
INTRODUCTION
Legumes hold an important economic and social
place and have a definite environmental benefit in
the Mediterranean Basin, which is the area of dis-
tribution of several genera of this family, including
the Medicago L. genus. This genus includes 86
species (Small & Jomphe, 1989) and comprises sev-
eral sections and subsections, including the Inter-
textae (Urban) Heyn subsection (Small, 2011;
Coulot & Rabaute, 2013). Some taxa of the Inter-
textae show a morphological ambiguity, which
reflected in different classifications. Indeed, some
authors ascribe to the subsection 4 species, namely,
Medicago ciliaris (L.) Kroclc., M. intertexta (L.)
Mill., M. muricoleptis Tineo and M. granadensis
Willd. (Quezel & Santa, 1962; Lesins & Lesins,
1979; Small & Jomphe, 1989; Coulot & Rabaute,
2013) and others mention only 3 species, M. inter-
texta, M. muricoleptis and M. granadensis (Heyn,
1963; Ponert, 1973; Jauzein, 1995; Dobignard &
Chatelain, 2012; Tison et al., 2014). According to
482
Meriem Laouar & Aissa Abdelguerfi
the latter authors M. ciliaris is either a subspecies,
M. intertexta subsp. ciliaris (L.), Ponert, or a botan-
ical variety [M. intertexta var. ciliaris (L.) Camb,
Heyn] of M. intertexta.
The early observations on the distribution of
annual Medicago in relation with soil factors were
made by Trumble & Donald (1938) and Aitken &
Davidson (1954). Besides, the first work on autoe-
cology was carried out in Australia by Andrew &
Hely (1960). Thereafter, several studies were
performed, particularly in the regions of origins of
Medicago , which allowed the definition of the eco-
logical requirements of various species (Ab-
delguerfi et al., 1988; Ehrman & Cocks, 1988; Pros-
peri et al., 1989; Ehrman & Cocks, 1990; Abdelkefi
et al., 1992; Bounejmate, 1992; Bounejmate et al.,
1992a; 1992b).
For the most common taxa of the Intertextae
subsection, M. ciliaris and M. intertexta , autoe-
cology research was carried out, but most of that
research did not allow comparisons between the
two taxa since they were included in a single
species as indicated by Heyn (1963). The most spe-
cific study on these two taxa was carried out in Al-
geria (Abdelguerfi-Laouar et al., 2003) on 179 sites.
Besides, M. muricoleptis and M. granadensis are
poorly distributed and are reported in the literature
as rare taxa. Although they belong to the same sub-
section as M. ciliaris and M. intertexta , they are not
found in Algeria, Morocco, and Tunisia. The eco-
logical requirements of the two taxa are not yet
determined; they have only been reported in various
regions (Table 1).
Other factors, besides ecological ones, symbio-
sis for example, may affect the distribution of
legumes species. The species of rhizobia that nodu-
late the Medicago ssp. belong to the Ensifer (for-
merly Sinorhizobium ) genus and are S. meliloti
(Dangeart, 1926) and S. medicae (Rome, 1996).
One of the major characteristics of the rhizobium-
legume association is their host specificity. In gen-
eral, a given rhizobium species can only establish
an efficient symbiotic relationship with a limited
number of plant partners. Similarly, legumes
species can only be specific to a certain number of
rhizobium species. This coevolution is often ig-
nored in studies on the distribution and evolution of
legumes taxa. The Intertextae subsection taxa were
described as specific to S. medicae (Bena et al.,
1998; 2005). Bena et al. (1998) suggest, for this
subsection, a recurrent loss of the capacity to form
an efficient symbiosis with strains of the S. meliloti
species; they hypothesize a punctual mutation
inducing a modification of the mechanisms of
recognition such as the flavonoid structure.
The rather particular geographical distribution
of the four Intertextae subsection taxa, namely
those with a wide distribution and those with a
narrow distribution, needs clarification as to
whether this is due to an ecological adaptation
and/or to a specific taxon-rhizobium interactions;
this is the objectives of this work.
MATERIAL AND METHODS
Given the taxonomic ambiguity that exists
within the subsection of the Intertextae , we will use
the term taxon instead of species for M. ciliaris ;
synonym: M. intertexta subsp. ciliaris and M. inter-
texta var. ciliaris, M. intertexta, M. muricoleptis and
M. granadensis throughout the document.
Ecological data and origin of sites
The study is focused on taxa M. ciliaris, M.
intertexta, M. muricoleptis and M. granadensis. The
collected ecological data come from the Australian
Medicago Genetic Resource Centre (South Austra-
lian Research and Development Institute: SARDI),
a total number of 125 sites were surveyed in 17
Mediterranean countries and islands (Table 2). 13
sites of 125 are sympatric (sci and sig), one of
which is sympatric to M. intertexta and M. granaden-
sis (sig; Israel) and the other (12) are for M. ciliaris
and M. intertexta (sci). All the other sites are al-
lopatric (sc, si, sm and sg) and correspond only to a
species per site among the four (Table 3).
Ecological data analysis
Nine (9) ecological characters were studied;
they correspond to orographic (altitude and slope),
climatic (annual rainfall) and edaphic characters
(pH, soil texture, soil depth, soil reaction, type of
drainage and land use). Analyses of variance
(ANOVA) with a single factor (sites) were carried
out on 76 sites whose data on rainfall, altitude, and
pH were available; the 'site' factor was considered
as random effect. The software used is STAT-ITCF
Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 483
Species
Regions
M. Lilians (L.) All.
- Macaronesia
Madeira Island (Portugal), Canary Island
(Spain)
- North Africa
Algeria, Egypt, Morocco, Tunisia
- Western Asia
Cyprus, Iraq, Israel, Lebanon, Western
Syria, Western Turkey
- South-Eastern Europe
Greece (including Crete), Italy (including
Sardinia and SicilvJ
- South-Western Europe
France (including Corsica), Portugal and
Spain (including the Balearic Islands)
- Macaronesia
Canary Island (Spain)
- North Africa
Northern Algeria, Morocco, Tunisia
M. intertexta (L.)
- South-Eastern Europe
Mill.
Greece, Italy (including Sardinia and
Sicily)
- South-Western Europe
France (including Corsica), Portugal and
the South of Spain
M. granadensis
Willd.
- North Africa
Northern Egypt
- Western Asia
Israel, Lebanon, Jordan, Western Syria,
Turkey
- South-Eastern Europe
M. muricoleptis
Southern Italy (including Sicily)
Tineo
- South-Western Europe
Southeast of the France near Toulon
References
Coulot & Rabaute, 2013
Davis, 1965-1988
Dobignard & Chatelain,
2012
Heyn, 1963
Jahandiez & Maire, 1931-1 941
Lesins & Lesins, 1 979
Meikle, 1977-1985
Mouterde, 1966
Pignatti, 1982
Pottier-Alapetite, 1979-1981
Quezel & Santa, 1962
Small & Jomphe, 1989
Small, 1981
Small et al., 1 98 1
Smyth ies, 1984-1986
Tackholm, 1974
Townsend & Guest, 1966
Tutin et al., 1 964- 1980
Zohary & Feinbrun- Dothan,
1966
GRIN, 2014
Table 1 . Geographical distribution of the Intertextae subsection taxa.
(Gouet & Philippeau, 2002). For each quantitative
variable, two analyses of variance were carried
out; the first analysis comprised 4 levels corre-
sponding to the presence of the taxon: (i) site of
M. ciliaris (sc+sci), (ii) site of M. intertexta
(si+sci), (iii) site of M. muricoleptis (sm) and (iv)
site of M. granadensis (sg+sig); the second analy-
sis (5 levels) differed from the first by the distinc-
tion of allopatric sites (12) from sympatric sites
for M. ciliaris and M. intertexta. For only those
where the null hypothesis is rejected a Fisher's
LSD test was calculated. The hypothesis is null
when the F test (MS A/MSE) of ANO VA is greater
than 1 (p <0.05).
For the qualitative variables, environmental pro-
files were established for each taxon having more
than five sites; the classes of each variable are rep-
resented in Table 4.
484
Meriem Laouar & Aissa Abdelguerfi
M.ciliaris : Algeria: 5.776 - 10.464 - 10.465 - 10.642 - 10.643 - 10.644 - 10.645 -
10.648 - 10.792 - 10.932- 10.933 - 10.934 - 10.935 - 10.936 - 11.571 - 11.574 -
11.575 - 11.576 - 12.547 - 12.551 . Crete : 2.081. Cyprus: 23 .627 - 23.629 - 23.635 -
23.636. Greece: 2.239. Israel: 2 .004 - 7.687 - 7.688. Italy: 2.075 - 5.782 - 22.419 -
22.420. Morocco: 25 .506 - 25.506 - 29.024. Portugal: 7.826 - 24.554 - Sardinia
26.016. Sicily: 2.067 - 2.186 -24.831 -24.844 - 24.847 - 24.849 - 24.852 - 24.853.
Spain: 7.721 - 28.255 - 28.256. Syria: 22 .206 - 24.022 - 24.023. Tunisia: 5.785 -
5.786 - 7.714 - 7.723 -10.637 - 18.460 - 18.463 - 18.464 - 20.104 - 21.802 - 21.803 -
21.804. Turkey: 23.932.
M intertexta : Algeria: 4.010 - 10.647 - 10.649 - 10.650 - 10.651 - 10.652 - 10.659 -
10.788 - 10.791 - 11.579 - 11.580 - 11.909 - 11.910 - 11.911 - 11.912 - 15.748.
Cyprus: 2.367 - 2.370 - 5.777. Egypt: 13.797 - 13.799. France: 2.044 - 2.045. Israel:
1.589 - 2.363 - 2.364 - 2.366 - 5.779. Italy: 2.071 - 2.375. Jordan: 18.084 - 19.002.
Morocco: 10.662. Portugal: 2.372 - 2,377 - 5.783 -8,323. Sardinia: 12.302 - 26.021.
Sicily: 24 .816 - 24.819 - 24.821 - 24.823 - 24.824. Spain: 1.590 - 2.361 - 2.362 -
28.257. Syria: 13.795 - 13.796. Tunisia : 4 .008 - 4.011 - 5.489 - 7.724 - 18.465
18.466.
M. granadensis : Israel: 2.359 - 5.778 - 5.822. Syria: 13.818 - 13.819 - 22.207.
Turkey: 23.928 -23.931 -26.380.
M. muricoleptis: Greece: 22.423. Italy: 15.343 - 22.422. Sicily: 24.825 - 25.026 -
25.027 -25.002.
Table 2. Collec-
tion of S ARDI.
Country
Allopatric sites
Sympatric sites
Total
M. ci liar is
(sc)
M. intertexta
(si)
M. muricoleptis
(sm)
M. granadensis
(sg)
M. ciliaris-
M. intertexta
(sci)
M. intertexta -
M. granadensis
(sig)
Algeria
15
11
-
-
5
-
31
Crete
1
-
-
-
-
-
1
Cyprus
4
3
-
-
-
-
7
Egypt
-
2
-
-
-
-
2
Spain
2
3
-
-
1
-
6
France
-
2
-
-
-
-
2
Greece
1
-
1
-
-
-
2
Israel
3
4
-
2
-
1
10
Italy
4
2
2
-
-
-
8
J ord an
-
2
-
-
-
-
2
Morocco
3
1
-
-
-
-
4
Portugal
1
3
-
-
1
-
5
Sardinia
1
2
-
-
-
-
3
Sicily
5
2
4
-
3
-
14
Syria
3
2
-
3
-
-
8
Tunisia
10
4
-
-
2
-
16
Turkey
1
-
-
3
-
-
4
Total
54
43
7
8
12
1
125
Table 3. Num-
ber of allopatric
and sympatric
sites by coun-
try.
Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 485
Collection of rhizobium strains
In a homogeneous site in Algiers (sub-humid,
soil with loamy texture and slightly alkaline pH),
8 populations, two by taxon, were planted. The pop-
ulations of M. granadensis and M. muricoleptis
originate from the Mediterranean collection
(SARDI) and those ofM ciliaris and M. intertexta
originate from an Algerian collection (ENS Ad’ Al-
ger). Populations ofM ciliaris (C58) and M. inter-
texta (158) from a sympatric site were taken into
account. On the generated seedlings, nodules were
collected from which a collection of 34 strains of
rhizobia was obtained (Table 5). Bacterial isolates
were obtained using the crushed-nodule method
(Vincent, 1970) from nodules removed from 60
days old plants. The various strains were stored in
glycerol at -80 °C, after having been identified by
a symbiotic test on M. polymorpha, in addition to
the analysis of 16S rRNA sequences (Rome et al.,
1996).
Extraction of DNA, Amplification by REP-
PCR and method of analysis
The DNA extraction was conducted following
the protocol of Abdelguerfi-Laouar (2005). The rep-
PCR and BOX-PCR was completed according to
the protocol of Rademaker et al. (1998). A primer
for BOX-PCR (BOX AIR: 5’-CTACGGCA-
AGGCGACGCTGACG-3’) and two primers for
REP-PCR (REP 1R: 5 MIIICGICGICATCIGGC-3 ’
and REP 21: 5MCGICTTATCIGGCCTAC-3’) were
used (Versalovic et al., 1994). The visualization of
bands was made by UV on long agarose gels at 1 .5
% (0.5X TBE) at 90 V voltage.
The binary data were established on the basis
of the presence (1) absence (0) of bands of REP
and BOX markers. From these data, a tree of
genetic distance was obtained by groupings of
plant from a comprehensive comparison of charac-
ters, then by calculating the mean distances of
grouped plants (NJ method: Neighbour Joining).
Support for clustering was determined by bootstrap
procedure applied on binary REP-BOX data (1000
replications). The software used is Dissimilarity
Analysis and Representation for Windows (DAR-
win) (Perrier et al., 2003; Perrier & Jaquemoud-
Collet, 2006).
Symbiotic Test
The two species S. meliloti and S. medicae rep-
resented by a 2011 strain and two ABS7 strains
(Bekki et al., 1987) and USDA1827, respectively,
were inoculated on the populations of the four taxa
of the Intertextae subsection. For symbiotic tests we
kept the same host populations that served to obtain
the collection of rhizobium. The seeds were disin-
fected with sulphuric acid for 30 minutes and then
germinated after flushing. After germination, each
seed was transferred, in sterile conditions, in tubes
containing the FAHRAEUS agar medium (1.5 %)
and placed in a culture chamber (20 °C, 60 % rela-
tive humidity and a photoperiod of 1 6 h light and 8
h darkness). The inoculation was carried out after
48 h of development of the roots (0.3 ml/seedling).
The notations begin after a week and end after 90
days. The experimental protocol used for the sym-
biotic tests is total randomization with three plants
per population.
RESULTS
Frequencies and geographical distribution
of taxa
The most frequent taxon of the Intertextae sub-
section in the Mediterranean region is M. ciliaris
with a frequency of 47.8 % followed by M. inter-
texta (40.6 %) and, finally, M. granadensis (6.5 %)
and M. muricoleptis (5.1 %). Of 17 Mediterranean
countries and islands, Algeria has the highest
frequency for M. ciliaris and M. intertexta. From
figure 1, which represents the distribution of 121
sites (longitude and latitude data available), M.
muricoleptis and M. granadensis are confined in
two restricted and different regions: the North and
the East of the Mediterranean, respectively. These
two taxa are included in the area of distribution of
M. ciliaris and M. intertexta.
By comparing the presence of taxa by countiy
between the bibliographic data (Table 1) and the
collection studied (Table 2, Fig. 1) similarities and
differences can be noted. In the Collection SARDI,
M. ciliaris was not collected in Egypt, Iraq, France,
and Lebanon; the same is true for M. intertexta in
Crete, Greece and Turkey. M. muricoleptis was not
collected in France and M. granadensis was not col-
486
Meriem Laouar & Aissa Abdelguerfi
lected in Egypt, Jordan, and Lebanon. Contrarily to
the literature, M. ciliaris andM intertexta were col-
lected in Israel; M. intertexta was collected in
Egypt, Cyprus, and Jordan; these two taxa therefore
exist in these countries.
Inter-taxa ecological variability
Rainfall, altitude and pH
The comparison among M. ciliaris, M. inter-
texta, M. muricoleptis and M. granadensis shows
that, with regard to altitude and pH, few differ-
ences exist (Table 6). Only rainfall allows differ-
entiating between the sites of M. ciliaris, M.
intertexta, sympatric sites (M. ciliaris and M.
intertexta ) (Table 7), M. granadensis and the sites
of M. muricoleptis. This latter taxon prefers the
highest rainfalls that exceed 800 mm. M. granaden-
sis has the lowest rainfall average of all the sub-
section.
To have an idea about the limits of adaptation
of each taxon, minimum and maximum values of
each character and each taxon were taken into con-
siderations. M. intertexta shows very broad adap-
tation for its precipitation needs; it shows the
biggest amplitude with 850 mm (Fig 2). It manages
to grow in dry conditions (150 mm, a single site in
Jordan) as well as in very wet conditions (1000
mm), but given the average for this character, it is
more frequent in the rainy areas. M. granadensis
and M. ciliaris are the least demanding in terms of
precipitation. M. muricoleptis is water demanding
as it is only found in sites with more than 700 mm
of rainfall (Fig 2). In altitude, minimum and maxi-
mum values are very close in the four taxa; they
vary from 5 to 10 m for low altitudes and from 900
to 1000 m for higher values. Sympatric sites of M.
ciliaris and M. intertexta show an average rainfall
closer to the average for M. intertexta than to the
average for M. ciliaris.
Edaphic characters (Texture, drainage,
depth of soil and soil reaction)
The soil textures in the sites of the four taxa are
fine; they are clayey or clay-loam. The loamy tex-
ture is specific only to M. ciliaris, M. intertexta and
M. granadensis (Fig. 3). The Intertextae taxa are
found both in soils with good water drainage and
soils where water stagnates on the surface. Only M.
intertexta shows 100%, in relative frequency, for
the class of submerged soil (waterlogged) (Fig. 4)
it is the only taxon that was not mentioned in the
W1C
N43
42
41
40
39
33
37
33
35
34
33
32
il
8 6 4 2 0 2 4 6 8 10 12 14 16 18 20 21 22 24 26 28 30 32 34 36 38E
i
m
i
c
i
c i
m
m
c i
ci
m
c
c i
c m
e
c i
c
c
c
c
c i
i
c i
c i
c i
cig
i
c
c
•g
i
i
Figure 1. Geographical distribution of Intertextae subsection taxa (121 sites) by longitude and latitude. The rectangle is 1 x
2 degrees [1 line: North Latitude (N: 3 1 to 42); 2 column: East Longitude (E: 0 to 38) and West (W: 0 to 10)]. Abbreviations
: c, M. ciliaris ; i, M. intertexta', g, M. granadensis', m, M. muricoleptis.
Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 487
Figure 2. Minimum, average, and maximum values of annual average rainfalls by taxon.
class with more than 40 cm of depth (Fig. 5). M.
ciliaris and M. intertexta can develop in soils that
are not very deep (10 cm). M. muricoleptis and M.
granadensis prefer deep soils.
M. granadensis does not seem to withstand
soil salinity considering its total absence in this
type of soil (Fig. 6). Owing to the absence of data
on soil reaction, M. muricoleptis was not studied.
Although this data is qualitative, ecological pro-
files confirm the resistance of M. ciliaris and M.
intertexta to salts as they are present in various
sites qualified as salty. Although the variance anal-
ysis did not highlight significant differences for
the pH, from ecological profiles of the soil reac-
tion character (Fig. 6) there are preferences de-
pending on the taxon. All of the three taxa M.
ciliaris , M. intertexta and M. granadensis grow
on alkaline soils. M. granadensis is the only one
present in sites with neutral soils and M. intertexta
confirms its presence on acid soils. Acid soils,
with a pH of 5, characterize only a few sites of M.
ciliaris and M. intertexta. By contrast, neutral and
alkaline soils are suitable for the four taxa of the
subsection.
Slope and Land Use
M. ciliaris and M. intertexta prefer flat grounds
in contrast to M. granadensis , which prefers slop-
ing grounds (16-30%). M. muricoleptis is interme-
diary with a preference for flat to undulating
ground (Fig. 7). The four taxa of the Intertextae
subsection are found in cultivated and grazed soils
and only M. ciliaris, M. intertexta andM granaden-
sis are found on roadsides (Fig. 8). M. ciliaris and
M. granadensis are more frequent on roadsides and
M. intertexta is more frequent in cultivated lands.
Unlike other taxa, M. muricoleptis is found more
often in pastures.
Symbiotic responses
The endemic taxa, M. muricoleptis and M.
granadensis, just as the taxa of M. intertexta and M.
ciliaris, are exclusively nodulated, in Algeria. The
inoculation of 34 trapped strains of rhizobia on M.
polymorpha showed an efficient nodulation
Nod+/Fix+ on all tested plants. This result confirms
that all collection of rhizobium is S. medicae.
488
Meriem Laouar & Aissa Abdelguerfi
Figures 3-8. Ecological profiles indicate the relative frequency of the taxon in the different classes (for class limits see
Table 4). Figure 3: soil texture. Figure 4: soil drainage. Figure 5: depth. Figure 6: soil reaction. Figure 7: slope. Figure
8: land use.
Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 489
The inoculation of the reference strain 2011 S.
meliloti shows that onM truncatula (A17) all the
plants nodulate and are efficient. No taxon of the
Intertextae nodulated efficiently with this strain. M.
ciliaris and M. intertexta do not show any nodule.
M. ciliaris offers the highest percentage of bumps
and M. granadensis shows the highest percentage
of Nod-. In M. granadensis and M. muricoleptis
non efficient nodules were formed on a small num-
ber of plants (Fig. 9). The strain ABS7, obtained
from M. ciliaris, nodulates efficiently, without ex-
ception, all the plants of the Intertextae subsection.
Variables
Abbreviation
Class codes
Classes
Texture
Tex
Texl-Tex3
Clay, loamy, loamy -clay
Drainage
Drn
Drnl-Drn4
Good soil drainage, free flow, Stagnation in
surface. Submersion
Depth (cm)
Dpth
Dpthl -Dpth3
0-1 0, 20-40 and +40 cm
Soil Reaction
Ret
Rctl -Rct4
Acidic, Neutral, Alkaline, Saline
Slope (%)
Sip
Sip 1-Slp3
0-3 % Flat, 3-8 % hilly, 16-30 % sloping
Land Use
LU
LU1-LU3
Crops, grazing, roadside
Table 4. Upper Limits of qualitative variable classes used for ecological profiles.
Taxon
Population
Code
Altitude
(m)
Rainfall
(mm)
Origin
Rhizobia Strains
M. ciliaris
DZ.C242
242
980
450
Algeria
3 Strains: DZ.c242.G3.1 ; DZ.c242.G3.2 ;
DZ.c242.G3. 3
M. ciliaris
DZ.C58
58
860
649
Algeria
3 Strains: DZ.c58.G1.2, DZ.c58.G1.4,
DZ.c58.G 1.5
M. intertexta
DZ.I331
331
880
1053
Algeria
5 Strains: DZ.i331 .G2.1 ; DZ.i33 1.G2.2;
DZ.i33 1.G2.3 ; DZ.i33 1.G2.4 ; DZ.i331.G2.5
M. intertexta
DZ.I58
58
860
649
Algeria
5 Strains: DZ.i58,G2.1, DZ.i58.G2.2,
DZ.i58.G2.3, DZ.i58.G2.4 DZ.i58.G2.5
M. granadensis
DZ.GAUS98
5.822
200
550
Israel
5 Strains: DZ.GAUS98.1.1, DZ.GAUS98. 1.2,
DZ.GAUS98.1.3, DZ.GAUS98.1 .4,
DZ.GAUS98.1.5,
M, granadensis
DZ.GAUS105
23.928
950
600
Turkey
5 Strains: DZ.GAUS 105. 1. 1, DZ.GAUS 105. 1.2,
DZ.GAUS 1 05. 1 .3, DZ.GAUS 1 05. 1 .4,
DZ.GAUS 105. 1. 5
M. muricoleptis
DZ.MAUS.l 10
24.825
630
800
Sicily
5 Strains: DZ.MAUS.l 10. 1 .1 , DZ.MAUS. 1 10. 1.2,
DZ.MAUS.l 10.1 .3, DZ.MAUS.l 10.1.4,
DZ.MAUS.l 10.1.5
M. muricoleptis
DZ.MAUS.107
25.028
5
700
Italy
3 Strains: DZ.MAUS.107. 1 .1 DZ.MAUS.107,1.3,
DZ.MAUS. 107. 1.4
Table 5. Collection of 34 rhizobia of Intertextae obtained by trapping.
490
Meriem Laouar & Aissa Abdelguerfi
Factors
Rainfall
Altitude
pH
Sites
Number
of sites
Average
(mm)
Number
of sites
Average
(m)
Number of
sites
Average
M. ciliaris
(sc+sci)
34
585.88 b
34
278.24
16
7.98
M. intertexta
(si+sei)
30
621.83 b
30
249.50
8
7.73
M. granadensis
(sg)
5
530.00 b
5
398.00
4
7.90
M. muricoleptis
(sm)
7
835.71 a
7
333.57
3
7.17
Meaning
-
* *
-
ns
-
ns
LSD = 1.996
Table 6. Comparison between environmental factors of the sites of Medicago ciliaris, M. intertexta, M. granadensis andM
muricoleptis. The letters a and b: indicate average groups. P(t), t-test on the groups of average [ * * * : p < 0.001; * * : P <
0.01; * : P< 0.05 ;n.s:P> 0.05 ].
Factors
Rainfall
Altitude
PH
Sites
Number
of sites
Average
(mm)
Number
of sites
Average
(m)
Number,
of sites
Average
M. ciliaris (sc)
22
571.82 b
22
288.41
13
7.84
M. intertexta (si)
18
628.61 b
18
242.78
5
7.20
M. granadensis (sg)
5
530.00 b
5
398.00
4
7.90
M. muricoleptis
(sm)
7
835.71 a
7
333.57
3
7.17
Mixed M. ci-M. ini
(sm)
12
611.67 b
12
259.58
3
8.60
Meaning
-
* *
-
ns
-
ns
LSD = 1.98
Table 7. Comparison between environmental factors (3) of sites with Medicago ciliaris alone, M. intertexta alone, M.
granadensis , M. muricoleptis and mixed sites withM ciliaris and M. intertexta. The letters a and b: indicate average groups.
P(t), t-test on the groups of average [ * * * : p < 0.001; * * : P < 0.01; * : P < 0.05 ; n.s: P > 0.05 ].
By contrast, USDA1827 (obtained from M. trunca-
tula) nodulates neither M. muricoleptis nor M.
granadensis. It nodulates one population of each
taxon of M. intertexta and M. ciliaris. Indeed, the
USDA1827 is specific within the species M. trun-
catula, for it nodulates some populations and not
others.
Genetic diversity of the trapped rhizobia
The electrophoresis of rep-PCR and BOX-PCR
revealed 114 bands (we only took intense bands) of
which 45 are monomorphic and the remainder is
made up of polymorphic bands. Polymorphism is
more frequent in M. granadensis strains with 55.5%
Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 491
of polymorphic bands, followed by M. intertexta
strains (50%); it is less than 25% in the other taxa.
We did not find specific bands that differentiate the
strains of the 4 taxa. Genetic distances (Fig. 10)
show a structuring of the strains of S. medicae by
forming 2 different groups. The first group (Gl)
corresponds to the strains that nodulate M. ciliaris
and M. intertexta and the second group (G2) is the
one trapped in M. granadensis and M. muricolep-
tis. There are 2 strains of M. granadensis of the
population DZ.GAUS98, which come together
with those of M. intertexta. Symbiotic specificity
is clearly established among widespread taxa and
endemic ones.
DISCUSSION
Geographic distribution
In the Mediterranean Basin, the four taxa, which
have a close relationship (Rose et al. 1988), show
different types of distributions: (i) endemic and rare
represented by M. granadensis and M. muricoleptis,
(ii) widespread and common represented by M.
ciliaris and M. intertexta. These results confirm
those obtained by several authors (Table 1). The
new data is that M. ciliaris and M. intertexta are
present in other countries that were never men-
tioned before in the literature. M. ciliaris is present
in Israel and M. intertexta in Israel, Egypt, Cyprus,
and Jordan. M. ciliaris is the most frequent in the
Mediterranean basin and particularly in Algeria. In
this country, this taxon is ranked fifth (163
sites/564) (Abdelguerfi, 2002).
Contrary to M. ciliaris, in the south west of the
Mediterranean M. intertexta is rare; it is absent in
the Northwest of Algeria and in the arid areas
(Abdelguerfi-Laouar et al., 2003). M. muricoleptis
is present in very restricted areas, Toulon in France
and Sicily in Italy. Nevertheless (according to
Coulot & Rabaute, 2013), the presence ofM muri-
coleptis in Toulon (France) is accidental, endemic
in the north Mediterranean, from the south of Italy
to Greece and M. granadensis is more confined to
western Asia, endemic in the East of the Mediter-
ranean and only adventitious in Europe and Chile.
Contrary to what mentioned by Small et al. (1999),
M. granadensis coexists with M. intertexta as the
two taxa were found together on a site.
Ecological requirements
M. muricoleptis is the most demanding water of
the Intertextae. Its geographic distribution corre-
sponds perfectly with this need. In Morocco, M.
intertexta and M. ciliaris were found only in the
areas with high rainfall and are confined to the areas
with mild winter and summer (Bounejmate et al.,
1992a, 1992b; Bounejmate, 1996). This does not re-
flect their requirement in the Mediterranean basin.
The Intertextae is known for its preference for
heavy and humid soils (Small et al., 1999). In
Algeria, M. ciliaris, M. intertexta, M. rigidula and
M. scutellata prefer heavy soils and M. ciliaris
grows particularly on marly soils (Abdelguerfi,
2002). Considering the specificity of the texture of
the Intertextae, the taxa should withstand soils with
poor water drainage. Indeed, the results show that
the taxa are found both in soils with good water
drainage and soils where water stagnates on the sur-
face. M. intertexta is the most adapted to hydromor-
phic soils, is considered one of the most tolerant to
waterlogging of the Annual Medicago genus (Fran-
cis & Poole, 1973). The waterlogging and salinity
are associated characters in the Mediterranean basin
(Kepner et al., 2005). The tolerance of plants to this
condition is due to a combination of anatomical,
physiological and morphological adaptations
(Predeepa-Javahar, 2012). OnlyM ciliaris and M.
intertexta are present in salt soil. Therefore we may
conclude that these two taxa are adapted to salinity.
Indeed, genotypes originating from salty soils are
often considered as tolerant, that is the conclusion
of Ben Salah et al. (2010) when they compared
under saline conditions (100 mmol of NaCl) two
pure lines originating from two different sites, one
rich in salt, and the other poor.
In Morocco, Bounejmate et al. (1992a; 1992b;
1994) and Bounejmate (1996) found the two taxa
in soils low in phosphorous, hydromorphic and
salty. According to Abdelkrim (1995), M. ciliaris is
found in fallows and idle lands with soils that are
colluvial, heavy, mostly marly and clayey, poorly
drained and more or less salty. M. ciliaris is classi-
fied as glycophyte and found in association with
halophyte species (Abdelly et al, 2006; Merabet et
al., 2006; Barret-Lennard & Setter, 2010). Other
research confirmed the adaptation of these taxa to
salinity (Greenway & Andrew, 1962; Lachaal et al.,
1995; Cherifiet al., 2011).
492
Meriem Laouar & Aissa Abdelguerfi
M. truncotulo
M. granodensis
M. muricoleptis
M. intertexta
M. ciliaris
0 % 20 % 40 % 60 % 80 % 100 %
■ Nod+/Fix-
l Nod+/fix+
lj Nod-
B Bump
Figure 9. Symbiotic responses to the inoculation of the reference strain 2011 S. meliloti in the taxa of the Intertextae sub-
section. Abbreviations : Nod +, nodulating phenotype; Nod + /fix+, nodulating phenotype-fixer; Nod-, non nodulating
phenotype; Bump, non nodulating root bulge.
Figure 10. Un- weighted neighbour-joining tree based on the simple matching dissimilarity matrix of REP and BOX markers
across the 34 strains of rhizobia trapped in a common site to all taxa in the subsection Intertextae. The numbers on the tips
indicate bootstrap values (expressed in percentages) and are shown for all clusters with >50 % bootstrap support. Abbre-
viations: c, M. ciliaris ; i, M. intertexta', m, M. muricoleptis', g, M. granadensis .
Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 493
Furthermore, some studies have shown that the
frequency of M. intertexta diminishes when the
pressure of pasture increases (Piano, 1987). Piano
et al. (1991) noted thatM ciliaris andM intertexta
are more frequent in cultivated lands.
Symbiotic response of M. granadensis and
M. muricoleptis in an exotic site
The various populations of M. granadensis and
M. muricoleptis nodulated efficiently in the Alge-
rian common site. The fact that M. granadensis
and M. muricoleptis nodulated efficiently with
rhizobia natives of Algeria, shows that their ab-
sence is not related to a restrictive coevolution
plant-rhizobium in this region. On some species,
particularly cultivated ones, a clear evolution was
noted between the species and its symbiote and
one of the more interesting examples is the pea,
which may form an efficient symbiosis with
strains of rhizobium from its site of origin in Tur-
key, but not with strains from other parts of this
country (Lie et al., 1987).
Taxonomic determination of the trapped
collection of Rhizobia
M. muricoleptis , M. granadensis, M. intertexta
and M. ciliaris are exclusively nodulated by the
strains of S. medicae, which confirms the results of
Bena et al. (1998) on the Intertextae subsection and
the results of Zribi et al. (2007) on M. ciliaris.
Indeed, in the trapping site, there were different
species of Medicago that were only nodulated by S.
meliloti including species of the Melilotus Mill,
genus. This confirms the specificity between the
subsection of the Intertextae and S. medicae. A re-
cent study (Epstein et al., 2012), comparing the two
genomes of S. medicae and S. meliloti, showed that
horizontal exchanges were almost exclusively of
plasmid genes and that the divergence between the
two species resulted from episodes of recent selec-
tion pressures.
Maybe it is not very correct to believe that this
specificity, whether for M. polymorpha or the sub-
section of the Intertextae, is related only to the host.
Indeed, other mechanisms affect the chemical struc-
ture of the synthesized Nod factors and therefore
prevent the nodulation (Van Rhijin & Vanderleyden,
1995; Denarie et al., 1996; Long, 1996). Alfalfa, for
example, is only nodulated in the presence of
sulphated Nod factors. This specificity mechanism
is based on the presence or absence, depending on
bacterial strains, of some genes that control the
synthesis of specific substitutes or their transfer on
the common skeleton. Other than genetic factors,
exogenous factors can influence the symbiosis
either for the choice of rhizobia that nodulate the
plant or for their efficiency.
According to Garan et al. (2005), S. medicae
nodulate more the species of Medicago that are
adapted to acid soils; by contrast, M. meliloti forms
a more frequent symbiosis with those that grow on
alkaline to neutral soils. This result does not apply
to the 4 taxa of the Intertextae subsection, since
they rather prefer alkaline to neutral soils.
Symbiotic specificity
The symbiotic response is not limited to the
presence or absence of nodules. Others structures
can exist and appear visually on the roots in the
form of more or less developed protuberances. Ge-
nerally, these forms do not grow bigger in length,
in fact, their development stops quickly. The study
of the effect of the Nod factors of Rhizobium me-
liloti (equivalent to S. meliloti ) on cultivated al-
falfa revealed several structures, such as nodules
and other protuberances (Grosjean & Huguet,
1997) .
Therefore, the symbiotic response other than the
presence absence of efficient nodules cannot be
dissociated from genetic variations of the host plant.
In this sense, the Nod- of M. muricoleptis and M.
granadensis induced by S. meliloti shows the diffe-
rence of these taxa relative to M. ciliaris and M.
intertexta.
Furthermore, the strain USDA1827 shows a
specificity of inter- and intra-species host and it is
not the only one. The population ESI 03 of M.
polymorpha achieves an efficient symbiosis with
ABS7m, while the population F34003 does not
form any nodule with this same strain (Bena et al.,
1998) .
Genetic relation between rhizobium and
taxa
According to Martinez -Romero (2009), plant-
rhizobium coevolution is more oriented by the plant
494
Meriem Laouar & Aissa Abdelguerfi
than by the rhizobium; it is the plant that must con-
stantly select the strains with which it gets in sym-
biosis. This result shows that the taxa acquired
genetic differentiation. In Tunisia, the results of
molecular and enzymatic analysis did not show
strains-species specificity in indigenous strains of M.
sativa cv. Gabbes, M. scutelleta cv. Kelson, M. trun-
catiila and M. ciliaris (Jebara, 2001). Although M.
muricoleptis and M. granadensis do not share the
same areas of distribution, they select genetically
close strains of rhizobium that are different from the
ones of indigenous taxa, M. ciliaris and M. intertexta.
These results indicate cospeciation between the
rhizobia and the endemic and widespread taxa. Co-
speciation between the rhizobia and leguminous
plants is not clearly established. Some authors
indicate that there is little concordance between the
phylogeny of bacteria and the phylogeny of
legumes plants (Doyle, 1998; Bena et al., 2005);
others, on the contrary, find links between both
partners (Ueda et al., 1995; Wemegreen & Riley,
1999; Laguerre et al., 2001).
What is the effect of the two factors on the
geographical distribution of taxa?
When analyzing ecological data, it appears that
there are no conditions specific to either taxon.
Some variations were observed among taxa but are
not discriminating. Consequently, M. muricoleptis
and M. granadensis are not specific to some habi-
tats and the limit of their dispersion is not ecologi-
cal. According to Griggs (1940), climatic and
edaphic factors are not the primary causes of the
rarity of a species, but the primary cause is compet-
itiveness. Other biotic factors may come into play;
we have seen that symbiosis does not seem to be a
factor that limits the dispersion of endemic species
since they have grown and nodulated in Algeria
where they are naturally absent. Indeed, from a
study on the effect of symbiosis on the expansion
of the Medicago genus (Bena et al., 2005), it was
concluded that symbiotic specificity can influence
the distribution of the species of the Medicago
genus, but not to the point of influencing their level
of endemism.
In this case, M. muricoleptis and M. granadensis
show local endemism that generally results from
geographic and genetic isolation. The geographical
distribution of the 4 taxa may result from allopatric
speciation where the populations are first separated
geographically, which provokes a net decrease or a
stop of the genetic exchanges, and the progressive
accumulation of differences among the populations.
According to the phylogenetic results, that indi-
cate that M. ciliaris and M. intertexta evolved from
a common lineage and that M. intertexta evolved
independently and gave rise to M. muricoleptis and
M. granadensis (Rose et al., 1988), we may assume
that M. muricoleptis and M. granadensis are young
species (neoendemism) (Willis, 1922; Stebbins,
1980) compared with M. intertexta and M. ciliaris
and that over time they could extend to other areas.
As mentioned by Lamotte (1994), in allopatric spe-
ciation, populations may be confronted to different
environments allowing or provoking differential
adaptations.
CONCLUSION
Ecological factors did not explain why phylo-
genetically close taxa belonging to the same sub-
section have different geographical distributions,
one narrow and one wide. The ecological require-
ments of taxa are more or less similar demonstrat-
ing that this is not the factor limiting the
distribution of M. muricoleptis and M. granaden-
sis in the region of the Mediterranean. Either the
symbiosis is not a factor limiting the presence of
these taxa which perform an efficient symbiosis in
an area where are naturally absent. As against,
endemic and widespread taxa show selectivity in
symbiont (rhizobia strains) which confirms their
differences. Other factors, such as genetic pool of
taxa, should be investigated to clarify the distribu-
tion of the Intertextae.
ACKNOWLEDGMENTS
We thank S.J. Hughes (SARDI) for sending us
the ecological data and the collection of Intertextae ,
T. Huguet (ENSA Toulouse, now retired) for
helping us in achieving the symbiotic part, G.G.
Guittonneau (Univ. Orleans, now retired) for his
guidance and advice. This work was supported in
part by the Algerian-French cooperation (Tassili
project).
Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 495
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On the presence of Notodiaphana atlantica Ortea, Moro et
Espinosa, 20 1 3 in the Mediterranen Sea, with notes on Retusa
multiquadrata Oberling, 1 970 and Cylichna mongii (Audouin,
1 826) (Cephalaspidea Cylichnidae)
Pasquale Micali
viaPapiria 17, 61032 Fano, Pesaro-Urbino, Italy; e-mail: lino.micali@virgilio.it
ABSTRACT Notodiaphana atlantica Ortea, Moro et Espinosa, 2013 (Cephalaspidea Cylichnidae) is re-
ported from various localities of Western and Central Mediterranean. Records of Retusa mul-
tiquadrata Oberling, 1970 are listed and discussed, most of them are considered to be based
on N. atlantica. Possible synonymy between N. atlantica and R. multiquadrata is discussed,
but former name is preferred. Based on the study of material from Suez channel. Bulla mongii
Audouin, 1826 seems to be based on a very young specimen of the common species Liloa
curta (A. Adams in Sowerby, 1850), but as Audouin’s name is older, then Bulla curta shall be
considered synonym of Bulla mongii. Liloa mongii (Audouin, 1826) new combination is than
proposed.
KEY WORDS Bulla mongii', Notodiaphana atlantica ; Retusa multiquadrata', Mediterranean; Lessepsian.
Received 18.10.2014; accepted 23.11.2014; printed 30.12.2014
INTRODUCTION
The recently described species Notodiaphana
atlantica Ortea, Moro et Espinosa, 2013 (Cepha-
laspidea Cylichnidae) is here reported for the first
time in the Mediterranean Sea. In the Mediter-
ranean Sea have also been reported Cylichna
mongii (Audouin, 1 826) and Retusa multiquadrata
Oberling, 1970, two poorly known species, which
need to be clarified to avoid misuse of the name.
Mediterranean records of these three species, ob-
viously only those accompanied by a photo, are
discussed.
Notodiaphana atlantica Ortea, Moro et Es-
pinosa, 2013
2013. Notodiaphana atlantica - Ortea et al.: 17, fig.
4, pi. 1.
1972. Cylichnina multiquadrata - Nordsieck: 35,
pi. O XVI, fig. 18
1995. Retusa multiquadrata - Miklcelsen: 205, fig.
2E
2001. Cylichnina multiquadrata - Cachia et al.: 125,
pi. XX, fig. 7
2008. Cylichnina multiquadrata - Cecalupo et al.:
128, pi. 75 figs. 5-7 (not fig. 4)
Examined material. Jerba (Tunisia), -2/3 m, 6
sh. (Figs. 5, 12-16); Pace, 5 km north of Messina,
Sicily, -6 m, 1 sh., 2014, legit A. Villari (Fig. 6);
Augusta, north of Syracuse, Sicily, beached in the
harbour area, 1 sh., 1990, legit A. Villari; Linosa
500
Pasquale Micali
island, Sicily Channel, -10 m, 1 sh., 2013, legit P.
Micali; Cabo Negro, Tetouan, Morocco, -30m, lsh.
Remarks. N. atlantica is described based on
specimens from a wide area ranging from Bahamas
islands to Cuba and Canary islands, type locality is
not designated.
Authors widely discuss the Mediterranean
records, bearing also a photo, of C. mongii and R.
multiquadrata, to ascertain whether this species is
present in the Mediterranean. In particular Authors
refer to the photos of three specimens in a work pub-
lished on web (http://www.naturamediterraneo.
com/forum/topic. asp?TOPIC_ID=l 00306) by the
Gmppo Malacologico Livornese and later on pub-
lished in the “Notiziario S.I.M.” (Gruppo Malaco-
logico Livornese, 2004), ignoring that the three
photos have been taken from Cecalupo & Quadri
(1996). Authors note that one of the three specimens
(they do not indicate which one, but possibly that
at photo lb) resembles N. atlantica for the profile
and the presence of spiral and axial threads. Authors
are misled by the indication that the figured speci-
men is 2.2 mm high and 1 .5 mm wide and conclude
that it is not N. atlantica for the size and the H/W
of 1 .46 against 2 in N. atlantica. Really Cecalupo
& Quadri (1996) determine the three specimens as
C. cfr. mongii and indicate that the specimen at fig.
1 is 2.2 mm high, while the other two, whose height
is not indicated, but may be calculated from the
enlargement (x 25) indicated in the legend of the
table, should be 1 .7 mm (fig. lb) and 1 .24 mm (fig.
lc) high. Ortea et al. (2013) conclude that N.
atlantica is not present in the Mediterranean.
Nordsieck (1972) describes and draws a speci-
men from Le Franqui, type locality of the species.
The Author states ”nach Foto von Oberling ”,
therefore description and drawing are taken from a
photo of C. multiquadrata that Oberling sent to
Nordsieck, and this is proved by the dimension of
the drawn specimen, that is very close to that
indicated by Oberling.
Ortea et al. (2013) do not mention the work of
Cecalupo et al. (2008) on the malacofauna of Gabes
gulf, where are figured two specimens from various
localities of Kerkennah island, as C. multiquadrata ,
having height ranging from 3.2 to 3.4 mm, therefore
well mature. Photo of a living specimen clearly
shows that soft parts are white, with a large darker
zone hardly visible inside the shell. This colour cor-
responds with N. atlantica , for which a large dark
spot, corresponding to digestive gland is indicated.
The specimen in Cecalupo et al. (2008) is
clearly different by N. atlantica , and it is currently
under study.
Cachia et al. (2001) describe and figure C. mul-
tiquadrata , stating that few empty shells have been
found at Salina Bay, Malta. From the description
and drawing of a specimen 3.9 mm high, there is no
doubt that it is N. atlantica.
Vazzana (2010) lists C. cfr. mongii at Scilla
(Strait of Messina), without figuring it. Based on
reported findings of N. atlantica in this area and the
photos on web, where this species is also on sale,
there is no doubts that the records in the Strait of
Messina shall be referred to N. atlantica.
Therefore based on studied material and con-
firmed records, N. atlantica is widespread in the
western and central Mediterranean sea, up to south
France, Sicilian coasts, Malta and south Tunisia.
N. atlantica may be easily separated from Liloa
mongii for the much finer cancellate sculpture with
more than double number of spiral grooves. The
sculture of L. mongii is not cancellate, consisting of
spiral grooves and growth folders. In specimens
about 2.2 mm high N. atlantica has a nearly
straight, instead of regularly convex lateral shell
profile. Seen from the aperture the profile shows a
wider and more squared last whorl and columellar
lip extended over the umbilical rim. Columellar
profile is inclined but almost straight in the joint to
the whorl, while in L. curta the columella is short
and there is an angle, not covered by columellar lip.
The abapical margin is more acute and by trans-
parency it is visible the external cancellate sculp-
ture, while in L. curta the margin is squared, quite
straight and only some spiral grooves may be seen
from inside (compare Figs. 1,2 and Figs. 3, 4)
R. multiquadrata was described a first time
(Oberling, 1970) with the following description:
“De rares specimens sur la plage de la Franqui
[north of Perpignan, south France]. Forme en cylin-
dre trapu, un peu comme R. mammillata. Phil.,
mais avec sommer perfore. Sculpture reticulee de
sillon spiraux et transverses, comme pour R. crebis-
culpta Mtr., mais reseau plus dense que dans cette
espece. La columelle est fortement developpee” .
In one later work (Oberling, 1971) the species
is again described with more details “Un petit (1 %
x 1 mm.) Retusa, presque cylindrique quoique avec
Notodiaphana atlantica in the Mediterranen Sea, with notes on Retusa multiquadrata and Cylichna mongii (Cylichnidae) 501
Figures 1, 2. Liloa mongii, Great Bitter Lake (Suez channel), height 2 mm. Fig. 1: front view. Fig. 2: apical view. Figures
3-5. Notodiaphana atlantica, Jerba (Tunisia), height = 2.3 mm. Fig. 3: front view for comparison with Fig. 1. Fig. 4: apical
view. Fig. 5: front view. Figure 6. N. atlantica. Pace (Messina), height = 2.3 mm. Figures 7-11. Liloa mongii, Great Bitter
Lake (Suez channel). Fig. 7: height 4.6 mm. Fig. 8: height 1.4 mm. Fig. 9: height 3.7 mm. Fig. 10: height 2 mm. Fig. 11:
height 2.3 mm (same specimen of Fig. 1). Figures 12-16. N. atlantica, Jerba (Tunisia). Fig. 12: height = 4.5 mm. Fig. 13:
height =1.7 mm. Figs. 14-16: height = 3.3 mm. Fig. 14: front view. Fig. 15: apical view. Fig. 16: lateral view.
502
Pasquale Micali
tours quelque peu convexes; spire enfoncee, proto-
conque visible au fond du trou ainsi cree, tours
autour de celui-ci-embrassants. Columelle tres
allongee (longueur pres de % de celle de la region
parietale); surface de la coquille treillissee de stries
spirales et verticales bien marquees. - Cette espece
ressemble vaguement au R. crebisculpta Mtrs.:
celui-ci est relativement deux fois plus long, sa
columelle beaucoup plus courte, sa protoconque est
cryptique, etc...”. The description fits with N. at-
lantica, but without the study of type material, even
after Nordsieck’s illustration of the species, the
name should be considered nomen dubium.
The name Cylichnina multiquadrata is used by
Mikkelsen (1995) for specimens from Azores, by
Buzzuito & Greppi (1997) in a list of shells from
Tasugu (south Turkey), without any comment or
figure and, later on, by Cecalupo et al. (2008) who
figure three specimens as C. multiquadrata , basing
the determination upon Oberling’s description. As
proved below, the specimens at figures 5-7 shall
actually be referred to N. atlantica, while specimen
at fig. 4, which is a little different, could be another
species.
It is astonishing that a species poorly described
and not figured, has met such a success. The type
material (not the holotype, which was not fixed)
seems to be lost (Oliverio in litteram, 08 Sept.
2014).
From what above seems that C. multiquadrata
and N. atlantica are synonyms, anyway as the spec-
imen figured by Nordsieck is not indicated as
belonging to type series, then C. multiquadrata is
here considered nomen dubium and N. atlantica is
the name to be used until Oberling’s type material
will be traced and studied.
Liloa mongii (Audouin, 1826) new combination
1826. Bulla mongii - Audouin: 39 (ref. to Savigny’s
figure, 1817: pi. 5, fig. 7).
1869. Cylichna mongii - Issel: 170 n° 424; 347 (ref.
to Savigny’s figure at pi. 5, fig. 7).
1926. Cylichna mongii - Pallary P.: 76, pi. 5, fig. 7.
1939. Cylichna mongei (sic) - Moazzo: 135.
1982. Bulla mongii - Bouchet & Danrigal: 14, fig.
58.
1996. Cylichnina cfr. mongii - Cecalupo & Quadri:
110, tav. Ill, fig. 1, la, lb.
2008. Liloa curta - Rusmore-Villaume: 150, fig.
2014. Liloa curta - Too et al.: 383, fig. 1 J (living),
3D, 17A-I
For further figures of L. curta see Too et al. (2014).
Examined material. Great Bitter lake, Suez
Channel, Egypt, legit G.P. Franzoni, 10 sh.
Remarks. Cylichna mongii (Audouin, 1826) is
a species of controversal determination, with many
records in literature (see below). At present not all
Authors agree on the origin or determination of
this species. Go fas & Zenetos (2003) list among
the species excluded from CIESM the C. cf.
mongii , with a “(w)” to indicate that “ citation is
considered to proceed from a misidentification of
a native species ”.
The difficulty in the determination of this
species is because Audouin (1826) assigned the
name of Bulla mongii to the species figured by
Savigny (1817) at pi. 5, fig. 7, therefore the species
was never described and Savigny’s drawing is very
small.
Issel (1869) indicates that the species is known
to him only from fossil specimens collected on
beaches above sea level (“, spiagge emerse del Golfo
Arabico”), but as the species was figured by Savi-
gny, it is then included among the recent species.
Issel (1869) gives the first description, obviously
based on his interpretation of the species: “ Conchi -
glia assai piccola, sottile, ovato-cilindrica, piii
ristretta alia parte inferiore che alia superiore,
bianca, liscia, non striata ne solcata, poco nitida;
apice incavato, non perforato. Apertura stretta, piii
allargata in basso che in alto; margine destro
regolarmente arcuato, semplice, superante l ’apice
alia parte superiore; parte visibile della columella
assai breve e non troncata. Dimensioni; Altezza
millim. 2; diametro 1 [shell very small, thin, ovate-
cylindrical, more restricted in the lower than in the
upper part, white, smooth, not striated or sulcate,
not glossy; spire sunken, not perforated. Aperture
narrow, larger in the lower than in the upper part;
right margin regularly arched, acute, protmding the
apex; visible portion of the columella very short,
not truncate. Dimensions: height 2 mm, width 1
mm]”.
Pallary (1926) does not add any comment. Lamy
(1938) reports this species for Ismailia (Suez
Notodiaphana atlantica in the Mediterranen Sea, with notes on Retusa multiquadrata and Cylichna mongii (Cylichnidae) 503
Channel), without comments. Moazzo (1939)
reports it for the bay of Suez and lake Timsah.
Bouchet & Danrigal (1982) illustrate the single spec-
imen, only 1 .6 mm high, present in Savigny collec-
tion, to be then considered the holotype. From the
photo it is possible to see the spiral lines present all
over the shell and the straight and folded outwardly
columellar lip.
From the comparison of type specimen and
Issel’s description, it is clear that Issel’s interpreta-
tion of this species is wrong, because he describes
the surface as smooth, not striated or sulcate.
Ortea et al. (2013) show the type specimen, after
metal coating, in little different position from photo
in Bouchet & Danrigal (1982), with a more realistic
view of the columellar profile and aperture.
Cecalupo & Quadri (1996) figure as C. cf. mongii
three specimens from Kyrenia (North Cyprus),
stating that this is the first Mediterranean record.
The CIESM (http://www.ciesm.otg/atlas/appendix
3bis.html, last update: December 2003) includes C.
cf. mongii (Audouin, 1 826) in the “List of excluded
species”, with the following comment: “ The taxon
reported under this name, from Cyprus by Cecalupo
and Quadri (1996), may be an undescribed
Mediterranean species. According to Van Aartsen
(pers. comm.) this species is also known from the
Island of Djerba, Tunisia, and Akkum, Turkey, and
without doubt lives in the Mediterranean”.
Cossignani & Ardovini (2011) figure the C. cf.
mongii using the photos from Cecalupo et al.
(2008), from Kerkennah (Tunisia), instead of those
from Cecalupo & Quadri (1996), showing the spec-
imens from Cyprus, to which is referred the com-
ment in CIESM (see above). In addition it is
erroneously indicated Malaga as origin of the
material.
The reduced size of the holotype (H= 1.6 mm)
let one suppose that it could be the immature stage
of a species living in the area. Studying the speci-
mens of Liloa curta (A. Adams in Sowerby, 1850)
collected in the Great Bitter Lake, it became clear
that Bidla mongii is based on an immature speci-
men of the species known as L. curta. Figures 7-
11 show a growth series from a specimen
corresponding to type of Bulla mongii, to a speci-
men corresponding to Liloa curta. The shell profile
varies with the growth, as the sculpture, which is
more evident in small specimens. As the Audouin’s
name is much older than Adams ‘s name, then the
new combination Liloa mongii (Audouin, 1 826) is
here proposed. This species shall be considered a
true Lessepsian migrant, as it is present in the Suez
Channel since long time and has entered the
Mediterranean.
L. curta, as such, has not been reported in the
Mediterranean sea, but record of C. mongii from
Cyprus by Cecalupo & Quadri (1996) shall be
considered the first in Mediterranean. Comparison
between L. mongii from Suez Channel and speci-
mens from Cyprus has been carried out with posi-
tive result.
L. mongii is a well known species with very
wide distribution covering Red Sea, Malaysia the
Philippines, China, Japan, Papua New Guinea,
Guam, New Caledonia and Hawaii (fide Too et al.,
2014). The description from Too et al. (2014) is the
following: “ Maximum height 18 mm; whitish; thin
and fragile, translucent, cylindrically oval, sides
slightly convex only, anterior end slightly rounded,
posterior end truncated; spire sunken, aperture
broad, outer lip thin, base semi-circular; spiral
grooves covering entire shell, distance between
spiral grooves almost equal, faint irregular axial
lines present”.
Moazzo (1939) reports this species as C. semisul-
cata Dunker, 1882 indicating it frequent in Lake
Timsah, less frequent in the Great Bitter Lake and
rare in Suez bay. Rusmore-Villaume (2008) in her
work on the Egyptian Red Sea, indicates L. curta
as “ infrequent in all areas. Locally common in shell
grit”, reaching a height of 12.5 mm. Studied speci-
mens from Great Bitter Lake reach about 5 mm.
Atys porcellana Gould, 1859, C. semisulcata and B.
curta A. Adams in Sowerby, 1850 are then syn-
onyms of B. mongii Audouin, 1826.
L. mongii may be easily separated from Atys
cylindricus (Hebling, 1779) for the depressed
spire, with a smaller protrusion between the spire
and lip, for the more cylindrical profile and the
spiral grooves covering the whole height of the
spire.
ACKNOWLEDGEMENTS
I thank Gian Paolo Franzoni (Tortoreto Lido,
Italy) and Alberto Villari (Messina, Italy) for the
submission of material, Marco Oliverio (Rome,
Italy) for the information on Oberling type material,
504
Pasquale Micali
Morena Tisselli (S. Zaccaria, Italy) for the biblio-
graphic support, Alberto Cecalupo (Milan, Italy) for
the comparison of specimens and Stefano Bartolini
(Florence, Italy) for the photos.
REFERENCES
Audoin V., 1826. Explication sommaire des planches de
Mollusques de F Egypte et de la Syrie publiees par
J.C. Savigny. Description de l’Egypte ou recuil des
observant et des recherches qui ont ete faites en
Egypte pendant F expedition de l’armee franqaise
publie par les ordres de sa majeste Fempereur
Napoleon le grand. Histoire Naturelle. Imprimerie
imperiale, Paris. Animaux invertebres, 1(4): 7-56.
Bouchet P. & Danrigal F., 1982. Napoleon’s Egyptian
Campaign (1798-1801) and the Savigny collection of
shells. The Nautilus, 96: 9-24.
Buzzurro G. & Greppi E., 1997. The Lessepsian mol-
lusca of Tasugu (South East Turkey). La Conchiglia,
Annuario 1996, Supplemento al n° 279: 3-22.
Cachia C., Mifsud C. & Sammut P.M., 2001. The marine
Mollusca of the Maltese Islands. Part Three.
Backhuys Publishers, Leiden, 182 pp.
Cecalupo A., Buzzurro G. & Mariani M., 2008. Con-
tribute alia conoscenza della malacofauna del Golfo
di Gabes (Tunisia). Quademi della Civica Stazione
Idrobiologica di Milano, 31: 1-175.
Cecalupo A. & Quadri P, 1996. Contributo alia
conoscenza malacologia per il nord dell’isola di
Cipro (Terza e ultima parte). Bollettino Malaco-
logico, 31: 95-118.
Cossignani T. & Ardovini R., 2011. Malacologia Mediter-
ranea. L’lnformatore Piceno, Ancona, 536 pp.
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Mediterranean basin: current status and perspectives.
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Gruppo Malacologico Livornese, 2004. Documenti del
Gruppo Malacologico Livornese. Notiziario S.I.M.,
22: 60-76.
Issel A., 1 869. Malacologia del Mar Rosso, ricerche zoo-
logiche e paleontologiche. Biblioteca Malacologica,
Pisa, 387 pp.
Lamy E., 1938. Mission Robert Ph. Dollfuss en Egypte:
7. Mollusca testacea. Memoires de Flnstitut
d’Egypte, 37: 1-90.
Mikkelsen P.M., 1995. Cephalaspid opisthobranchs of
the Azores. In: Martins A.M.F. (Ed.), The marine
fauna and flora of the Azores. Proceedings of the
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Moazzo P.G., 1939; Mollusques testaces marins du Canal
du Suez. Memoires de Flnstitut d’Egypte, 38: 1-283.
NordsieckF., 1972. Die Europaischen Meeresschnecken.
Gustav Fischer Verlag. Stuttgart, 327 pp.
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pris de microgasteropodes Mediterraneen. Kleine
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& Ortea, 2004 (Gastropoda: Opisthobranchia: Cepha-
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Biodiversity Journal, 2014, 5 (4): 505-508
The first earthworm records from Malta (Oligochaeta Lum
bricidae)
Csaba Csuzdi 1 & Arnold Sciberras 2 *
'Department of Zoology, Eszterhazy Karoly Coollege, Eger, Hungary; e-mail: csuzdi.csaba@ektf.hu
2 1 33 'Arnesf , Arcade Str, Paola, Malta; e-mail: bioislets@gmail.com
* Corresponding author
ABSTRACT The first earthworm report from Malta lists seven species; six species from the Holarctic family
Lumbricidae and one species from the Mediterranean family Hormogastridae. Apart from the
Circum-Mediterranean Octodrilus complanatus (Duges, 1828) and the Trans-Aegean
Octodrilus transpadanus (Rosa, 1884) the other four lumbricid species recorded are widely
distributed peregrine. The unidentified hormogastrid specimen might represent an au-
tochthonous species in Malta.
KEY WORDS Earthworms; fauna; new record; Maltese Islands.
Received 23.10.2014; accepted 01.12.2014; printed 30.12.2014
INTRODUCTION
Earthworms (Oligochaeta Lumbricidae) repre-
sent one of the most important groups of the soil
fauna. Due to the earthworms’ activity not only the
structure of the soil is altered, but also the chemical
composition is substantially changed (Lee, 1985).
As members of the saprophagous guild, earth-
worm species play a paramount role in the decom-
position of dead plant material (litter, dead grass,
etc.) in temperate forests (Zicsi, 1983). Their activ-
ity is also important in the tropical regions as well,
where, together with termites, earthworms are re-
sponsible for the decomposition of 40% of dead
plant material (Lee, 1985).
This is the reason why earthworms are con-
sidered “soil ecosystem engineers” (Jones et al.,
1994; Decaens et al., 2001), which play a funda-
mental role in maintaining soil fertility and con-
sequently are indispensable for sustainable agricul-
ture (Jimenez et al., 2001). Contrary to their vital
importance in biogeochemical cycles we have de-
tailed ecological data only about two dozen species
(Zicsi et al., 2011) from the some 800 valid lum-
bricid species distributed over the Holarctic
(Csuzdi, 2012).
In addition, there are regions even in Europe
from where earthworm records are scarce or com-
pletely missing.
One of such region is Malta from where, up to
our present knowledge, there are no earthworm
records published. In the last year the second
author, a herpetologist interested in different lizard
groups investigated the available prey-population
including earthworms in Malta.
During this short-term study five earthworm
species have been recorded which, together with
some other specimens from the collection of the
Hungarian Natural History Museum, are herewith
presented.
506
Csaba Csuzdi & Arnold Sciberras
MATERIAL AND METHODS
A larger study collecting all fauna present in
sampling sites was being carried out in two pre-
vious separate studies.
One of the authors (AS) resident on Malta, was
able to monitor, dig and hand sort the mentioned
retrieved specimens along with his colleague
Patrick Vella. Along with the latter specimens from
the Hungarian Natural History Museum, all speci-
mens were studied by CC and included in the
current list.
All voucher specimens that have been collected
are now housed in the collection of one of the
authors (CC).
RESULTS
Family LUMBRICIDAE Rafmesque-Schmaltz, 1815
Allolobophora chlorotica (Savigny, 1826)
Enterion chloroticum Savigny, 1826: 182.
Allolobophora chlorotica : Csuzdi & Zicsi,
2003: 50 (for complete synonymy).
Examined material. SantaMarija bay, Comino
Island (Maltese Archipelago), 3 adult ex., 1 adult
and 1 juvenile ex., 3 adult ex., leg. A. Sciberras.
Aporrectodea trapezoides (Duges, 1828)
Lumbricus trapezoides Duges, 1828: 289.
Aporrectodea trapezoides : Blakemore, 2008:
531 (for complete synonymy).
Examined material. 23 adult ex., 1 adult ex.,
Chadwik Lakes, 1 adult ex., leg. V. Mahnert,
06.V.1974.
Aporrectodea rosea (Savigny, 1826)
Enterion roseum Savigny, 1826: 182.
Aporrectodea rosea : Csuzdi & Zicsi, 2003: 92
(for complete synonymy).
Examined material. 1 adult ex., 1 adult and 1
juvenile ex., Around St. Georges Bay under stones,
in Garrique, 1 adult ex., leg. V. Mahnert, 04.V.1974.
Eiseniella tetraedra (Savigny, 1826)
Enterion tetraedrum Savigny, 1826: 184.
Eiseniella tetraedra : Csuzdi & Zicsi, 2003: 153
(for complete synonymy).
Examined material. Chadwik Lakes, 1 adult
ex., leg. V. Mahnert, 06.V.1974.
Octodrilus complanatus (Duges, 1828)
Lumbricus complanatus Duges, 1828: 289.
Octodrilus complanatus : Blakemore, 2008: 625
(for complete synonymy).
Examined material. 6 adult and 5 1 juvenile ex.
Octodrilus transpadanus (Rosa, 1884)
Allolobophora transpadana Rosa, 1884: 45.
Octodrilus transpadanus : Csuzdi & Zicsi, 2003:
215 (for complete synonymy).
Examined material. Around St. Georges Bay
under stones, in Garrique, 1 adult ex., leg. V.
Mahnert, 04.V.1974.
Family HORMOGASTRIDAE Michaelsen, 1900
Hormogaster sp.
Examined material. 1 juvenile ex.
Remarks. We have only one juvenile specimen
representing this Mediterranean family Hormoga-
stridae, therefore, the exact species identification is
not possible.
DISCUSSION
This small sample from Malta consisted of
seven earthworm species of which four lumbricids
The first earthworm records from Malta (Oligochaeta Lumbricidae)
507
(A. chlorotica, A. rosea , A. trapezoides and E.
tetraedra ) are widely distributed, peregrines which
most probably were introduced by human activi-
ties. The other two lumbricid species ( O . com-
planatus and O. transpadanus ) possess more
restricted area (Circum-Mediterranean and Trans-
Aegean respectively) however, they are also capa-
ble for human introduction (see e.g. Mischis et al.,
2005; Blakemore, 2008).
The only species which can be endemic in the
island is the unidentified Hormogaster species.
Hormogaster are distributed over the Western
Mediterranean basin (Omodeo & Rota, 2008) and
seemingly have no tendency for human introduc-
tion. Consequently, the presence of this species in
Malta can be connected with the island’s geologi-
cal history.
The Maltese islands are situated on a shallow
shelf called Malta-Ragusa Rise extending from the
Ragusa Peninsula of Sicily toward the African
coast (Magri et al., 2008). The presence of many
Siculo-Maltese endemic species proves the close
biogeographic relationships between Malta and
Sicily which is a consequence of land connections
with Sicily either in the Quaternary or in the
Messinian stage of the Miocene Epoch (Hunt &
Schembri, 1999).
Therefore, the abundant presence of Hormo-
gaster redii Rosa, 1887 in Sicily (Omodeo & Rota,
2008) provides an apparent explanation of the ori-
gin of Hormogaster in Malta, however to draw
more specific conclusions exact species identifica-
tion is needed.
ACKNOWLEDGEMENTS
The authours wish to thank Patrick Vella,
Esther Sciberras, Jeffrey Sciberras, Romario
Sciberras for their assistance in field work and
Prof. Patrick J. Schembri for assistance in litera-
ture search.
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508
Csaba Csuzdi & Arnold Sciberras
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Biodiversity Journal, 2014, 5 (4): 509-514
Alvania dalmatica Buzzurro et Prkic, 2007 (Gastropoda Ris-
soidae): range extension, shell variability, habitat and relation-
ships with A. hallgassi Amati et Oliverio, 1 985
Luigi Romani
Via delle ville 79, 55013 Lammari, Lucca, Italy; e-mail: luigiromani78@gmail.com
ABSTRACT Shell samples of Alvania dalmatica Buzzurro et Prkic, 2007 (Gastropoda Rissoidae) were
obtained from Corfu. This is the first record of the species from the Ionian Sea and Greece.
The shells show a wide morphological variation not previously reported for the species.
Numerous shells of A. hallgassi Amati et Oliverio, 1985 were also found in the same localities.
Some unreported features of this species are pointed out and the relationships with A. dalmatica
are considered.
KEY WORDS Rissoidae; Alvania; variability; Mediterranean Sea; new findings.
Received 10.11.2014; accepted 01.12.2014; printed 30.12.2014
INTRODUCTION
Alvania Risso, 1826 (Gastropoda Rissoidae) is
a rissoid genus represented in the Mediterranean
Sea by more than 70 species (Gofas, 2014). Its in-
trageneric relationships are still largerly unresolved,
lacking large-scale investigations on anatomical and
molecular grounds. Some widely distributed and
polymorphic taxa are probably complex of cryptic
species while others often form quite uniform
groups of species with not clear interspecific bound-
aries. Most of the latters have been recently de-
scribed with very limited ranges.
Alvania dalmatica Buzzurro et Prkic, 2007 was
described from some Dalmatian islands (Croatia),
from bottoms rich of Corallium rubrum (Linnaeus,
1758) (Buzzurro & Prkic, 2007), no further records
are known.
It is closely related, on conchological grounds,
to A. hallgassi Amati et Oliverio, 1985 and A. di-
aniensis Oliverio, 1988. All these species occur in
central Mediterrenean and share a paucispiral pro-
toconch sculptured with spiral threads and an ovate-
conical teleoconch with a reticulated pattern,
formed by the intersection of spiral and axial sculp-
tures which are comparable in size.
Alvania hallgassi is known from Ionian coasts
of Southern Italy and Sicily (Amati & Oliverio,
1985; Oliverio et al., 1986; Giannuzzi-Savelli et al.,
1997; Trono, 2006; Cossignani & Ardovini, 2011;
Scuderi & Terlizzi, 2012) and reported from central
Tyrrhenian Sea (Scaperrotta et al., 2012). Alvania
dianiensis is distributed along Tyrrhenian coasts
from southern France to Sicily and recently found
in northern Adriatic Sea (Oliverio, 1988; Buzzurro
et al., 1999; Cossignani & Ardovini, 2011; Micali
& Siragusa, 2013; pers obs.).
Relying on published data, the three species can
be characterized by shell morphology, habitat and
distribution, as reported in Table 1 .
510
Luigi Romani
Alvania dalmatica
Alvania hallgassi
Alvania dianiensis
Total height
2. 6-3. 5 mm
2-2.3 mm
2-2.4 mm
Teleoconch whorls
3.6
3
3.2
Number of axial ribs on
the last whorl
16-17
15-30
14-23
Spiral cords on the last
whorl
7-9
8-11
6-7
Spiral cords above
the aperture
4-5
4-7
3
Denticles in the
outer lip
Yes
No
No
Protoconch whorls
1.4
1.5
1.5
Protoconch spiral
threads
6-7, running throughout
its extension
5-6, the nucleus with only
the first and last threads
5-6, running throughout its
extension
Protoconch interspaces
smooth
smooth
papillose
Colour
Background light yellow
with two small darker bands
(one sutural and one basal)
Background yellow with two
darker bands (one sutural
and one basal)
Whitish-yellowish, uniform
Habitat
Corallium rubrum
photophilic algae
photophilic algae
Depth
60-90
down to 20
18-48
Distribution
Dalmatian coasts
Ionian Sea
Tyrrhenian and Ligurian seas
Table 1. Characters of Alvania dalmatica, A.hallgassi, A. dianiensis from literature.
MATERIAL AND METHODS
All shells were found in bottom samples col-
lected by SCUBA diving. The protoconch whorls
are counted according to the method as described
by Verduin (1977).
Examined material. A. dalmatica. 4 shs from
Lastovo Island (Croatia), 60-90 m, in CBC and
SBC; 80 shs from Skeloudi Island (Paleokastritza,
Corfu, Greece), 40-50 m, Kolowri island (Pale-
okastritza, Corfu, Greece), 53 m, Liapades reef off
Cape Agios Iliodoros (Liapades, Corfu, Greece),
45 m, in SBC and ARC.
Alvania cf. hallgassi- dalmatica. About 40 shs
from the aforementioned Corfu localities, dates
and collectors, in SBC and ARC; about 15 shs
from Lastovo Island (Croatia), 40 m, in SBC.
Alvania hallgassi : holotype (MCZR); more
than 180 shs from the aforementioned Corfu local-
ities, dates and collectors, in SBC and ARC; about
200 shs from Punta Campanella and Scoglio
Vervece (Naples, Italy), 50 m, in SBC and ARC;
about 150 shs from Lastovo Island (Croatia), 40
m, in SBC; 6 shs from Gallipoli (Lecce, Italy), 80
m, in CBC; 2 shs from Torre Suda (Lecce, Italy),
82 m, in APC; 4 shs from Cannizzaro (Catania,
Italy), 35 m, in LRC; 2 shs from Scilla (Reggio
Calabria, Italy), 50 m, in LRC.
Alvania dianiensis. some hundred shs from
Palinuro (Salerno, Italy) 30 m, in SBC and CBC; 8
shs from Giglio Island (Grosseto, Italy), in SBC and
CBC; 15 shs from Cres (Croatia), 36 m, in ESC.
Alvania oliverioi. 10 shs from Protaras (Cyprus),
25 m, in SBC and CBC; 2 shs from N Cyprus, 2-6
m, in CBC.
Alvania dalmatica (Rissoidae): range extension, shell variability, habitat and relationships with A. hallgassi
511
ABBREVIATIONS AND ACRONYMS. APC:
Attilio Pagli collection (Lari, Italy); ARC: Alessan-
dro Raveggi collection (Florence, Italy); CBC:
Cesare Bogi collection (Livorno, Italy); FSC:
Franco Siragusa collection (Livorno, Italy); LRC:
Luigi Romani collection (Lucca, Italy); SBC: Ste-
fano Bartolini collection (Florence, Italy); MCZR:
Zoological Museum Rome, Italy; shs: shells.
DISCUSSION
Alvania dalmatica original description was based
on the holotype, with no mention of the other shells’
features (except size), so the morphological vari-
ability of the species cannot be properly assessed.
It’s however supposed to be veiy limited. Despite the
low number of the examined topotypical shells, they
match very well with the original description and
show a great uniformity (Table 2, Figs. 1-8).
The greek shells share all diagnostic characters
with topotypical A. dalmatica : paucispiral proto-
conch sculptured by spiral threads and smooth in-
terspaces (Fig. 13); teleoconch with quite regular
cancellate sculpture, axial microsculpture on the
surface among spiral and axial ribs, outer lip inter-
nally lirate and thickened. While the protoconchs
are very uniform in the two samples, the teleo-
conchs show a far greater variability previously
unreported, both in size, sculpture and colour (Table
2, Figs. 1-8). Measured shells are fully developed
adult (labial lirae and varix present) but their av-
erage size is lower than topotypical ones, altough it
varies considerably.
Shells outline is more or less slender (Figs. 5,
8), while the number of labial lirae is regularly
lower, probably due to the smaller size. The genesis
of the spiral chords follows the same pattern in both
samples: two chords starting immediately after
metamorphosis, later a third chord rising between
them; finally in a few specimens a fourth and/or a
fifth chord appearing. The teleoconch sculpture is
highly variable due to the interaction between axial
and spiral elements: from coarse and sparse (Figs.
2, 5, 7) to quite delicate and close-set (Fig. 6).
The number of spiral cords is on average lower
compared to the Croatian shells but the appearance
of the 3rd one is far more variable as well as well
as the number of axial ribs. Consequently the spiral
cords above the aperture numbering from 2 (Fig. 2)
to 4 (Fig. 4) or 5 (Fig. 6), most commonly 3 with
an incipient subsutural chord (Fig. 3). The intersec-
Alvania dalmatica
Croatia (4 shs)
Alvania dalmatica
Greece (70 shs)
Total height
3.2-3. 5 mm
2.3-3. 1 mm (average 2.7 mm)
Teleoconch whorls
3.7-4
3.1-4 (average 3.5)
Number of axial ribs on the last whorl
16-17
13-22 (average 17.5)
3rd spiral cord appearance (whorl)
1.5-1. 7
1.3-2. 7 (average 1.9)
Spiral cords on the last whorl
8-9
5-9 (average 6.7)
Spiral cords above the aperture
4
2-5 (average 3)
Number of lirae in the outer lip
9-11
7-8
Protoconch diameter
400-410 pm
380-410 pm (average 400 pm)
Nucleus diameter
130-140 pm
130-140 pm
Protoconch whorls
1.4-1. 5
1.3-1. 5 (average 1.5)
Protoconch spiral threads
6-7
6-7
Table 2. Shell morphological features of Alvania dalmatica.
512
Luigi Romani
tions are generally nodulous, but varying from weak
and barely raised (Fig. 6) to strong and somewhat
spinous (Figs. 2,1). The cancellation from squarish
(Figs. 2, 3) to clearly rectangular (Figs. 7, 8). The
size and sculpture features appear substantially
continuous. The colour also is also not constant:
generally it is uniform whitish to caramel (Figs. 3,
4), some specimens are brownish (Fig. 8), others
have two faint subsutural and columellar hazelnut
bands (Fig. 7), or spiral cords more marked than
background colour (Fig. 5).
Up to now A. dalmatica range was restricted to
south-central Adriatic Sea, with the present note it
is extended 400 km southward into Ionian Sea. This
suggests a wider distribution probably overlooked
due to the confusion with other Alvania species.
Concerning the habitat, A. dalmatica was reported
in exclusive association with Corallium rubrum
and with a restricted bathymetrical range (60-90
m), here it is extended to 40 m depth and corallige-
nous bottoms. Surprisingly no A. dalmatica shells
were found in Lastovo Is., the type locality of the
species. The depth 40 m is shallower than that
reported for the type material but coincide with that
of A. dalmatica from Corfu.
A large population of A. hallgassi was found
simpatrically with A. dalmatica in Corfu. The
shells fit with the original diagnosis in some
respects: paucispiral protoconch (Fig. 14); general
outline; quite delicate, reticulate sculpture with
axial ribs ranging from 20 to 40 (most commonly
around 30) and 8-10 spiral cords on the body
whorl; outer lip relatively thin with a faint external
varix. Yet some features disagree: the total height
is on average greater, spanning from 2.4 mm to 3
mm; the protoconch size and sculpture are sub-
stantially identical to A. dalmatica with spiral
threads all beginning from the nucleus, not only
the first and last ones as stated in the original
description; the outer lip (in fully developed shells,
about 15% of the samples) has inner denticles
(lirae) yet weaker than A. dalmatica. The teleo-
conch sculpture is also quite variable and in some
shells is rather coarse (Figs. 9, 10). The genesis of
the spiral chords is very similar to A. dalmatica
but fourth and/or a fifth chords are present in most
shells (Figs. 9, 11).
The colour in most cases shows typical pattern:
two brown bands (a sutural and a basal) on a yel-
lowish background, but several shells are uni-
formly whitish-yellowish sometimes with spiral
cords darker.
To better place these characters in a more gen-
eral context, A. hallgassi shells from various south-
ern Italy localities were examined: The holotype is
a slightly worn shell with a pebble occluding the
aperture, so it is not very useful in order to examine
these features. But in two large samples very near
the type locality about 20% of fully developed
shells are lirate (50 shs from Punta Faci, 36 m, and
40 shs from Torre del Serpe, 25 m, both south of
Otranto, Lecce, Italy, Macri pers. com.). Alvania
hallgassi from Naples have typical size (maximum
2.2 mm) colour pattern, shell sculpture, but the pro-
toconch is identical to A. dalmatica and a small per-
centage of shells exibit weak denticles in the
aperture. Also A. hallgassi from Sicily share the
same protoconch and denticulation features (the
size of the sample is small, yet two specimens are
weakly lirate). It seems, therefore, that a protoconch
wholly marked by spiral threads biginning from the
nucleus and the presence af labial lirae in a small
percetange of adult shells are typical of the species.
CONCLUSION
Concluding, A. hallgassi and A. dalmatica share
some key diagnostic features (protoconch size/
sculpture and inner lip denticulation). On the other
hand, examining large samples, several specimens
of A. hallgassi and A. dalmatica come close in
terms of sculpture and colour in an apparent contin-
uous spectrum, so being difficult to attribute them
with certainty to each species (Figs. 6, 12); these
latter features indeed are so variable in each indi-
vidual that it’s difficult to use them for diagnostic
purposes. Also some A. hallgassi shells from
Lastovo Is., with particularly coarse sculpture, over-
lap with delicate-sculptured A. dalmatica.
A. dianiensis has a papillose protoconch surface,
no labial denticles and seems to have more uniform
shell sculpture, but Micali & Siragusa (2013) attrib-
uted to A. dianiensis a population from N Adriatic
Sea with a very coarse teleoconch sculpture, largely
different from the typical pattern of the species. So,
in this context, extensive investigations involving
also molecular tools, are desirable to better under-
standing the boundaries within A. hallgassi-dianen-
sis-dalmatica complex of species.
Alvania dalmatica (Rissoidae): range extension, shell variability, habitat and relationships with A. hallgassi
513
Figures 1-12. Alvania spp. Fig. 1. A. dalmatica, Lastovo is., Croatia, 3.3 mm; Figs. 2-8. A. dalmatica, Corfu, Greece, 2.6 mm
(2), 3.2 mm (3), 3 mm (4), 3 mm (5), 2.8 mm (6), 2.7 mm (7), 2.9 mm (8). Figs. 9-10. A. hallgassi, Corfu, Greece, 2.8 mm
(9), 3 mm (10). Fig. 11 .A. hallgassi, Lastovo is., Croatia, 2.9 mm. Fig. 12. A. hallgassi-dalmatica, Corfu, Greece, 2.8 mm.
514
Luigi Romani
Figure 13. Protoconch of A. dalmatica.
Figure 14. Protoconch of A. hallgassi.
ACKNOWLEDGEMENTS
I thank Alessandro Raveggi and Maria Scaper-
rotta who picked and sorted the sediment samples,
Alessandro Raveggi, Stefano Bartolini, Cesare
Bogi, Franco Siragusa, Attilio Pagli for loaning
their material and Stefano Bartolini for taking digi-
tal photographs and composing the plate. I’m grate-
ful to Gabriele Macri, Danilo Scuderi and Daniele
Trono who shared useful information. Bruno Amati
and Enzo Campani for suggestions and for critical
reading of the manuscript. Leonardo Fortunato
improved the english text.
REFERENCES
Amati B. & Oliverio M., 1985. Alvania ( Alvaniello )
hallgassi sp. n. Notiziario C.I.S.Ma, 6: 28-34.
Buzzurro G., Hoarau A., Greppi E. & Pelorce J., 1999.
Contributo alia conoscenza dei molluschi marini
della Rada d’Agay (Francia sudorientale). La
Conchiglia, 31 (291), 36-43, 61-62.
Buzzurro G. & Prkic J., 2007. Anew species of Alvania
(Gastropoda: Prosobranchia: Rissoidae) from
Croatian coast of Dalmatia. Triton, 15: 5-9.
Cossignani T. & Ardovini R., 2011. Malacologia Mediter-
ranea. Atlante delle conchiglie del Mediterraneo -
7.500 foto a colori. L’lnformatore Piceno, Ancona.
537 pp.
Giannuzzi-Savelli R., Pusateri F., Palmeri A. & Ebreo
C., 1997. Atlante delle conchiglie marine del
Mediterraneo. Vol. 2 (Caenogastropoda, parte 1:
Discopoda - Heteropoda). La Conchiglia Ed.,
Roma, 258 pp.
Gofas S., 2014. Alvania Risso, 1826. Accessed through:
World Register of Marine Species at http://www.
marinespecies.org/ aphia.php?p=taxdetails&id= 1384
39 on 2014-10-30
Micali P. & Siragusa F., 2013. Segnalazione di Alvania
dianiensis Oliverio, 1988 in Adriatico settentrionale.
Notiziario S.I.M., 31: 28-29.
Oliverio M., 1988. Anew Prosobranch from the Mediter-
ranean Sea , Alvania dianensis n. sp. Bulletin, Zoolo-
gisch Museum, Universiteit van Amsterdam, 11:
117-120.
Oliverio M., Amati B. & Nofroni I., 1986. Proposta di
adeguamento sistematico dei Rissoidaea (sensu
Ponder) del Mar Mediterraneo. Parte I: famiglia
Rissoidae Gray, 1847 (Gastropoda: Prosobranchia).
Notiziario C.I.S.Ma, 7-8: 35-52.
Scaperrotta M., Bartolini S. & Bogi C., 2012. Accresci-
menti. Vol. IV. L'lnformatore Piceno, Ancona. 185
pp.
Scuderi D. & Terlizzi A., 2012. Manuale di Malacologia
dell'Alto Jonio. Ed. Grifo, Lecce, 188 pp.
Trono D., 2006. Nuovi dati sulla malacofauna del Salento
(Puglia meridionale). Bollettino Malacologico, 42:
58-84.
Verduin A., 1977. On a remarkable dimorphism of the
apices in many groups of sympatric, closely related
marine gastropod species. Basteria, 41: 91-95.
Biodiversity Journal, 2014, 5 (4): 515-520
Mediterranean Umbraculida Odhner, 1939 (Gastropoda
Opisthobranchia): diagnostic tools and new records
Luigi Romani
Via delle ville 79, 55013 Lammari, Lucca, Italy; e-mail: luigiromani78@gmail.com
ABSTRACT Some diagnostic tools are given to distinguish juvenile shells of the Mediterranean Umbra-
culida Odhner, 1939 species (Gastropoda Opisthobranchia) and some new records of rare
species are added.
KEY WORDS juveniles; Mediterranean Sea; new findings; protoconch; Umbraculida.
Received 10.11.2014; accepted 01.12.2014; printed 30.12.2014
INTRODUCTION
The Umbraculida is a small order of opistho-
branchiate molluscs represented in the Mediter-
ranean Sea by 4 species and 2 families: Umbra-
culidae Dali, 1889 comprising Spiricella unguicu-
lus Rang, 1828 and Umbraculum umbraculum
(Lightfoot, 1786) and Tylodinidae Gray, 1847 with
Tylodina perversa (Gmelin, 1791) and Anidolyta
duebenii (Loven, 1846).
Tylodinella trinchesii Mazzarelli, 1897 is an
obscure entity put in synonimy with T. perversa but
still poorly understood (Waren & Di Paco, 1996;
Gofas, 2013).
All species share an uncoiled patelliform or
shield-like shells. Aside from anatomical differences
adult specimens can be easily identified by shell
features (Vayssiere, 1885; Pruvot-Fol, 1954; Waren
& Di Paco, 1996; Valdes & Lozouet, 2000; Cachia
et al., 2001; Da Silva & Landau, 2007) (Table 1, 2
and Figs. 1-9). Juvenile shells (except S. unguicu-
lus) instead are not easily distinguishable from each
other. Flere are provide some information on the
protoconch and early teleoconch morphology to set
some characters useful for specific determination.
MATERIAL AND METHODS
Examined Material. Umbraculum umbracu-
lum : 7 shs, 0.7 mm to 4 mm, Lamaca (Cyprus), 45
m, in ARC; 3 shs, 2.2 mm to 4.7 mm Corfu
(Greece), 40 m, in SBC; 2 shs, 35-65 mm, Isola
delle Femmine (Palermo, Italy), 30 m, SBC; 1 sh,
51 mm, Gorgona is. (Livorno, Italy), 70/80 m, in
ECC; 1 sh, 11.7 mm, Palinuro (Salerno, Italy) 30
m, in CSC; 1 sh, 11.5 mm, Acitrezza (Catania, Italy)
40 m, in CBC.
Spiricella unguiculus. 1 sh, 3.6 mm, Salina
(Messina, Italy), 35 m, in PPC; 1 sh, 2.7 mm, Pal-
inuro (Salerno, Italy), 35 m, in SBC; Castelsardo
(Sassari, Italy), 50 m, 2.6 mm, in CBC; 1 sh, 2.2
mm, Tarifa (Spain), 27 m, in CSC.
Tylodina perversa. 16 shs, Palinuro (Salerno,
Italy), 35 m, in SBC and CSC; 2 shs, Protaras
(Cyprus), 35 m, in SBC; 2 shs, Campomarino
(Taranto, Italy), in SBC; 1 sh, Krk is. (Croatia), in
SBC; 22 shs, Elba is. (Livorno, Italy), in SBC; 1 sh,
Capraia is. (Livorno, Italy), 260 m, in SBC;
Gorgona is. (Livorno, Italy), 150 m, in CSC; 1 sh,
Capraia is. (Livorno, Italy), 150 m, in CSC; lsh,
Almeria (Spain), 110 m, in APC; 2 shs, Capraia is.
516
Luigi Romani
(Livorno, Italy), 180 m, in APC. Shs ranging from
l. 5 mm to 25 mm.
Anidolyta duebenii. 3 shs, 5 mm, 3.2 mm and
3.1 mm, Almeria (Spain), 110 m, in APC and SBC;
1 sh, 3.3 mm, Scoglio Vervece (Naples, Italy), 51
m, in APC; 1 sh, 8.3 mm, Capraia is. (Livorno,
Italy), 300 m, in CSC; 2 shs, 1.3 mm and 3.2 mm,
Pianosa is. (Livorno, Italy), 400 m, in RRC.
ABBREVIATIONS AND ACRONYMS. APC:
Attilio Pagli collection (Lari, Italy). ARC: Alessan-
dro Raveggi collection (Florence, Italy). CBC:
Cesare Bogi collection (Livorno, Italy). CSC: Carlo
Sbrana collection (Livorno, Italy). ECC: Enzo
Campani collection (Livorno, Italy). PPC: Paolo
Paolini collection (Livorno, Italy). RRC: Romualdo
Rocchini collection (Pistoia, Italy). SBC: Stefano
Bartolini collection (Florence, Italy). sh(s): shell(s)
DISCUSSION
Umbraculum umbraculum juveniles (Figs. 10-
1 3) can be easily recognized by the protoconch size,
by far the largest of the considered species. It is quite
variable in size ranging from 630 pm to 710 pm
(average 670 pm) in maximum diameter, composed
by 1 .3-1 .5 whorls, globose (nucleus not prominent),
quickly expanding, glossy, thin and semitransparent,
colour light brown. A shallow depression is present
beyond the protoconch-teleoconch border. Shell up
to 3-4 mm, more elevated, somehow capuliform,
quite thin, of the same color of the protoconch, then
increasingly flat, greyish and thicker.
Spiricella unguiculus juveniles are unmistak-
able, having basically the same silhouette of adut
shells with the protoconch arranged in the horizon-
tal plane, adherent to the surface of the teleoconch.
Tylodina pervert juveniles (Figs. 14, 16, 19)
are similar in outline to U. umbraculum but the pro-
toconch is smaller, ranging from 360 pm to 400 pm
(aver-age 370 pm) in maximum diameter. It is com-
posed by 0.9-1 . 1 whorls, globose (nucleus not prom-
inent), not quickly expanding. It is quite protruding,
glossy, thick, not transparent, white or yellowish
uniform in colour. Teleoconch is thickened in apical
region becoming th inn er toward the margin, its
profile is very variable, from extremely flat to rather
conical. Colour varies from white to brownish. The
muscle scar marks are obvious and often make in-
ternal surface quite uneven.
Anidolyta duebenii juveniles (Figs. 15, 17, 18)
have a protoconch ranging from 350 pm to 400 pm
(aver-age 370 pm) in maximum diameter composed
by 0. 9-1.1 whorls, substantially comparable to T.
perversa in size and form, but some slight differ-
ences can be detected: the nucleus is tinged while
the remaining of the protoconch and teleoconch are
white, the protoconch whorl increases less than T.
perversa so the apex has apparently a more promi-
nent aspect, whit a clear “neck” on the protoconch-
Shell features
Umbraculum
umbraculum
Spiricella unguiculus
Tylodina perversa
Anidolyta duebenii
Size (average)
50-70 mm
4-7 mm
15-20 mm
8-10 mm
Outline
oval
subrectangular
oval
oval
profile
depressed
depressed, arched
Conical to depressed
regularly conical
apex
pointed, slightly
excentric
flat, strongly excentric
pointed, slightly
excentric
pointed, slightly
excentric
surface
dull, with only concen-
tric growth lines
Quite glossy, with only
concentric growth lines
glossy, with only con-
centric growth lines
glossy, with only con-
centric growth lines
colour
grey-yellowish
grey-yellowish
whitish-yellowish
white
Periostracum
Thick, felt-like, dark
brown
Thin, transparent
Thick, membranaceus,
purple-reddish, often
banded
thin, transparent
Muscle scar
Circular, discontinuous,
many strong scars
horseshoe-shaped
Circular, complete,
quite strong, with sinus
Circular, omplete, very
faint, no sinus
Table 1. Shell features of the Mediterranean Umbraculida (adult shells).
Mediterranean Umbraculida Odhner, 1 939 (Gastropoda Opisthobranchia): diagnostic tools and new records
517
Figures 1-3. Umbraculum umbraculum, isola delle Femmine, Palermo, Italy, 65 mm (Figs. 1, 2), 35 mm (Fig. 3).
Figs. 4-6. Tylodina perversa, Krk is., Croatia, 25 mm. Figs. 7-8. Anidolyta duebenii, Capraia is., Livorno, Italy, 8.3 mm.
Fig. 9. Spiricella unguiculus, Castelsardo, Sassari, Italy, 2.6 mm.
518
Luigi Romani
Figures 10-13. Umbraculum umbraculum juvenes, Corfu, Greece, 4 mm. Figures 14, 16, 19. Tylodina perversa juvenes,
Elba island, Italy, 1.8 mm (Fig. 14), 3.6 mm (Figs. 16, 19). Figures 15, 17, 18. Anidolyta duebenii juvenes, Almeria, Spain,
3.2 mm.
Mediterranean Umbraculida Odhner, 1 939 (Gastropoda Opisthobranchia): diagnostic tools and new records
519
teleoconch border. The teleoconch is more elevated,
regularly conical, uniformly thin. The muscle scar
forms a complete circle, it is very weak and almost
invisible.
Umbraculum umbraculum and T. perversa
young shells could be mistaken but protoconch size
is resolutive, also muscle scar sinus is important,
already visible in few mm specimens. T. perversa
and A. duebenii are obviously the most difficult
species to separate having the protoconch of the
same size but the colour of the nucleus and promi-
nence could be useful tools to distinguish them.
Moreover shell profile, thickness and muscle scars
help distinguishing also very small shells. Anidolyta
duebenii records are deeper than 100 m (the Naples
record is unusually shallow) but bathymetry is mis-
leading in order to separate it from T. perversa , as
dead specimens of the latter can be found at depths
greater than 250-300 m. Most A duebenii records
examined in collections are actually T. perversa orig-
inating from deep water.
Spiricella unguiculus is a very rare species, with
a lusitanian distribution, recorded in literature for
few scattered shells. It’s biology and ecology are
virtually unknown as no living specimens have
been found so far. Its systematic position in Umbra-
culidae is doubtful judging by shell characters and
only tentative lacking anatomical and molecular
data (Tringali, 1990; Da Silva & Landau, 2007 and
references therein; Cossignani & Ardovini, 2011).
With the present note its range is extended to
northern Sicily and southern Spain.
1 . Protoconch larger than 600 pm
Umbraculum umbraculum
- Protoconch smaller than 600 pm 2
2. Protoconch smaller than 350 pm, recumbent
Spiricella unguiculus
- Protoconch larger than 350 pm, raised 3
3. Protoconch color uniform, less promi-
nent Tylodina perversa
- Protoconch nucleus tinged, more promi-
nent Anidolyta duebenii
Table 2. Key of the Mediterranean Umbraculida
based on the protoconch features.
Anidolyta duebenii is an uncommon species
living in deepwaters, spanning from Norwegian Sea
to Lusitanian seamounts and Mediterranean Sea
(Waren & Di Paco, 1996; Beck et al., 2006). The few
mediterranean records are from Spain and Corsica
(Waren & Di Paco, 1996; Penas et al., 2006; Penas
et al., 2008). It’s now reported from Gulf of Naples
and confirmed from Northern Tyrrhenian Sea.
ACKNOWLEDGEMENTS
Stefano Bartolini, Cesare Bogi, Enzo Campani,
Attilio Pagli, Paolo Paolini, Alessandro Raveggi
and Carlo Sbrana are thanked for making available
material for this study. Marco Oliverio, Morena
Tisselli, Maurizio Forli and Maurizio Sosso for use-
ful discussion. A special thanks to Pasquale Micali
for his precious suggestions which clarified much
of my original doubts. I’m grateful to Stefano
Bartolini for taking digital photographs and com-
posing the plates.
REFERENCES
Beck T., Metzger T. & Freiwald A., 2006. Biodiversity
inventorial atlas of macrobenthic seamount animals.
Available online at: http://wwwl.uni-hamburg.
de/OASIS/Pages/publications/BIAS.pdf [Accessed:
30-10-2014],
Cachia C., Mifsud C. & Sammut P., 2001. The Marine
Mollusca of the Maltese Islands Part 3: Sub-class
Prosobranchia to sub-class Pulmonata, order Basom-
matophora. Backhuys Publishers, Leiden, 266 pp.
Cossignani T. & Ardovini R., 2011. Malacologia Mediter-
ranea: atlante delle conchiglie del Mediterraneo:
7500 foto a colori. Ancona, L'informatore Piceno.
536 pp.
Da Silva C.M. & Landau B.M., 2007. Cenozoic Atlanto-
Mediterranean biogeography of Spiricella (Gas-
tropoda, Umbraculidae) and climate change: filling
the geological gap. Veliger, 49: 19-26.
Gofas S., 2013. Umbraculida. Accessed through: World
Register of Marine Species at http://www.marine
species. org/aphia.php?p=taxdetails&id=3 82227 on
2014-10-30
Penas A., Rolan E., Luque A. A., Templado J., Moreno D.,
Rubio F., Salas C., Sierra A. & Gofas S., 2006. Molus-
cos marinos de la isla de Alboran. Iberus, 24: 23-151.
Penas A., Rolan E. & Ballesteros M., 2008. Segunda
adicion a la fauna malacologica del litoral de Garraf
(NE de la Peninsula Iberica). Iberus, 26: 15-A2.
520
Luigi Romani
Pravot-Fol A., 1954. Mollusques Opisthobranches.
Faune de France. Lechevalier, Paris. 58: 1-460.
Tringali L., 1990. Breve nota sul ritrovamento di due
interessanti micromolluschi nel Mar Tirreno. No-
tiziario C.I.S.M.A., 12: 13-16.
Valdes A. & Lozouet P., 2000. Opisthobranch molluscs
from the tertiary of the Aquitaine basin (South-West-
ern France), with descriptions of seven new species
and a new genus. Palaeontology, 43: 457-479.
Vayssiere A., 1885. Recherches zoologiques et
anatomiques sur les mollusques Opisthobranches du
Golfe de Marseille. Pt. 1, Tectibranches. Annales du
Musee d'Histoire Naturelle de Marseille, Zoologie 2,
Mem. 3: 1-181, pis. 1-6.
Waren A. & Di Paco G., 1996. Redescription of
Anidolyta duebeni (Loven), a little known notap-
sidean gastropod. Bollettino Malacologico, 32: 19-
26.
Biodiversity Journal, 2014, 5 (4): 521-524
New records of Ceratocanthinae (Coleoptera Scarabaeoidea
Hybosoridae) from Arunachal Pradesh (India) with descrip-
tion of a new species of Pterorthochaetes Gestro, 1 898
Alberto Ballerio
Viale Venezia 45, 25123 Brescia, Italy; e-mail: alberto.ballerio.bs@numerica.it
ABSTRACT In order to publish data to be included in the forthcoming new edition of the Catalogue of
Palaearctic Coleoptera, Madrasostes feae (Gestro, 1898) and Pterorthochaetes dembickyi
n. sp. (Coleoptera Scarabaeoidea Hybosoridae Ceratocanthinae) are recorded from Arunachal
Pradesh (India).
KEY WORDS Palaearctic region; Pterorthochaetes ; Madrasostes', new species.
Received 25.11.2014; accepted 09.12.2014; printed 30.12.2014
INTRODUCTION
After the publication of new data on Palaearctic
Ceratocanthinae (Coleoptera, Scarabaeoidea, Hy-
bosoridae) (Ballerio, 2014) to be included in the
forthcoming second edition of the Catalogue of
Palaearctic Coleoptera by Lobl and Smetana, some
new data on Ceratocanthinae from Arunachal
Pradesh (an Indian region belonging to the Palaearc-
tic region) were obtained by examining unidentified
material kept in ZFMK collection. The purpose of
this note is therefore to describe a new species of
Pterorthochaetes Gestro, 1898 and to provide new
faunistic data on Madrasostes feae (Gestro, 1898)
based on the aforementioned new Indian material.
Poggi (2010) demonstrated that the correct date
of publication of the names contained in Gestro's
revision of Asian Ceratocanthinae (which includes
also Pterorthochaetes and M. feae) is 1898 and not
1899, as previously reported.
MATERIAL AND METHODS
I refer to Ballerio (2013) and references therein
quoted for methods and terminological conven-
tions.
Habitus photographs were taken with a Canon
Eos D5 Mil with a macro objective MP 65 mm, all
photos were then mounted with the Zerene Stacker
software and cleaned and unmasked using a photo
processing software.
ABBREVIATIONS. EL: maximum elytral
length; EW: maximum total elytral width; HL:
maximum head length; HW: maximum head width;
L: length; PL: maximum pronotal length at middle;
PW: maximum pronotal width at middle; W: width;
ZFMK: Zoologische Forschungsmuseum Alexan-
der Koenig collection, Bonn, Germany.
RESULTS
Madrasostes feae (Gestro, 1898) (Fig. 1)
Examined material. 1 male and 1 female
(ZFMK): NE India, Assam- Arunachal border,
Bhalukpong, 150 m, 27°00'48"N 92°39'08 M E, L.
Dembicky leg., 1-8.V.2012.
522
Alberto Ballerio
Remarks. First record for Arunachal Pradesh.
Madrasostes feae was previously known from
Nepal, NE India (Uttarakhand, Meghalaya and
Sikkim), Myanmar, Thailand and Kampuchea
(Ballerio, 2014).
Pterorthochaetes dembickyi n. sp.
Examined material. Holotypus, male, in coll.
ZFMK: NE India, Arunachal Pr., Etalin vicinity,
700 m, 28°36'56"N 95°53'21"E, L. Dembicky leg.,
12-25.V.2012. Allotypus in ZFMK, same data as
holotypus.
Description of holotypus (Figs. 3-6). HL: 0.9
mm; HW: 1.8 mm; PL: 1.6 mm; PW: 2.9 mm; EL:
3.3 mm; EW: 2.9 mm. Large sized Pterorthochaetes,
surface shiny, setose; volant. Dorsum black, seta-
tion yellowish-brown, sternum reddish-brown, an-
tennae and tarsi reddish-brown. Head: subpen-
tagonal, wider than long, fore margin finely ser-
rated, tip acute, interocular distance about 10 times
the maximum width of dorsal ocular area, dorsal
ocular area large, dorsal sculpturing of head distally
made of very coarse and deep transverse wrinkles
and proximally of impressed small dense mixed
comma-shaped and horseshoe-shaped punctures
centrifiigally oriented, each one having a pore in the
internal side, bearing an erect simple short seta.
Pronotum: wider than long (W/L ratio= 1.8),
fore angles normally shaped, pronotal lateral mar-
gins fringed with a row of short simple setae,
spaced out by an interval about their length or
longer, disc of pronotum covered by dense im-
pressed ocellate transverse small punctures larger
at sides of disc and becoming horseshoe-shaped
large punctures, with opening outwards, towards
pronotal base and sides, each puncture with a pore
in the middle bearing a gently clavate medium sized
erect seta; punctation relatively dense, the distance
between punctures being subequal to their diameter
on disc and inferior to their diameter at sides.
Scutellum: punctures transversely horseshoe-
shaped, sparse, thick and coarse. Elytra: shape oval,
longer than wide (W/L ratio= 0.8); elytral surface
covered by dense punctation, made of medium
sized impressed horseshoe-shaped punctures with
opening directed outwards, horseshoe branches
short, punctures spaced out by an interval larger
than their diameter, horseshoe-shaped punctures
mixed with a few simple shallow small punctures
irregularly distributed. Each horseshoe-shaped punc-
ture containing a pore bearing a gently clavate long
erect seta.
Male genitalia: spiculum gastrale as in figure 1 1 ,
parameres asymmetrical, as in figures 7-9, internal
sac with an elongate narrow sclerite, as in figure 10.
Variability. Allotypus: overall morphology as
in the description of holotypus. Sexual dimorphism
as in all other Pterorthochaetes. Bursal sclerites
slightly asymmetrical, with a dorsal sharp projec-
tion and shaped as in figure 12.
Comparative notes. Pterorthochaetes dembickyi
n. sp. is mainly characterized by the shape of bursal
sclerites, shape of parameres and of the sclerites of
internal sac of aedeagus, which isolate the new
species from all other known Pterorthochaetes. As
regards outer morphology, the size, the setation of
pronotal margins and the punctation pattern of ely-
tra and pronotum allow us to place this new species
near P. septemtrionalis Ballerio, 1999 and P. yun-
nanensis Ballerio, 2014.
The new species can be easily distinguished
from P. septemtrionalis because the latter has
much denser and larger elytral punctation, elytral
horseshoe-shaped punctures have branches longer
and the opening is directed mainly backwards
(and not outwards as in the new species), while
differences from P. yunnanensis are subtler,
consisting in the shape and density of simple ely-
tral punctures: in P. yunnanensis they are much
more impressed and denser than in P. dembickyi
n. sp., also horseshoe-shaped punctures are
slightly denser and larger in P yunnanensis. The
strong differences in the shape of bursal sclerites
and, for P. septemtrionalis and P. dembickyi n. sp.,
in the shape of parameres and of sclerites of
internal sac of aedeagus (in P. yunnanensis the
male is unknown) do not allow any confusion be-
tween the new species and P. septemtrionalis and
P. yunnanensis.
Etymology. Noun in the genitive case. Dedi-
cated to Lubos Dembicky, who collected the type
series.
Distribution and Habitat. Known only from
the type locality in NE India (Fig. 2). The type
series was collected under the bark of dead trees (L.
Dembicky, pers. comm.), in a montane broadleaf
New records of Ceratocanthinae from Arunachal Pradesh (India) with description of a new species of Pterorthochaetes 523
Figure 1. Madrasostes feae , specimen from Figure 2. Pterorthochaetes dembickyi n. sp., type locality
Bhalukpong, habitus in dorsal view. (photo by L. Dembicky, 2012).
1 mm
Figures 3-6. Pterorthochaetes dembickyn n. sp., holotypus. Fig. 3: extended, dorsal view. Fig. 4: enrolled, ventral view.
Fig. 5: enrolled, dorsal view. Fig. 6: enrolled, lateral view.
524
Alberto Ballerio
Figures 7-10. Pterorthochaetes dembickyi n. sp., holotypus,
parameres. Fig. 7. Dorsal view, Fig. 8. Lateral view. Fig. 9.
Lateral view. Fig. 10. Internal sac (arrow indicates the elon-
gate sclerite).
Figure 11 .Pterorthochaetes dembickyn n. sp., spiculum gas-
trale of holotypus. Figure 12. Pterorthochaetes dembickyn
n. sp., bursal sclerites of allotypus (arrows indicate the dorsal
sharp projection).
forest near Etalin (Mishmi Hills), an area belonging
to the Eastern Himalayan broadleaf forests ecore-
gion (Wikramanayake et al., 2002).
Remarks. I examined other four females of
Pterorthochaetes (ZMFK) from the type locality,
which have bursal sclerites somewhat similar to the
ones of P dembickyi n. sp., although with dorsal
projections stronger, blunter and longer. The outer
morphology is quite different, the length is shorter
(about 1 mm shorter), elytral horseshoe-shaped
punctures are larger and pronotum has larger
horseshoe-shaped punctures at the sides, with open-
ing wider, and a few wrinkles near fore angles.
Based on what we know about intraspecific mor-
phological variation in the genus Pterorthochaetes ,
it is more likely that those females represent a dis-
tinct new species rather than an extreme variation
of P. dembickyi n. sp. Because of this I excluded
those females from the type series.
ACKNOWLEDGEMENTS
I would like to thank Dirk Ahr ens (ZFMK) and
Lubos Dembicky (Moravske zemske muzeum,
Brno, Czech Republic) for the loan of material and
information. Special thanks to Ignazio Sparacio
(Palermo, Italy) for editorial assistance.
REFERENCES
Ballerio A., 2013. Revision of the Australian Ceratocan-
thinae (Coleoptera, Scarabaeoidea, Hybosoridae).
ZooKeys, 339: 67-91.
Ballerio A., 2014. New data on Palaearctic Ceratocanthi-
nae with description of a new species from China
(Coleoptera: Scarabaeoidea: Hybosoridae). Koleopterol-
ogische Rundschau, 84: 277-280.
Gestro R., 1898. Sopra alcune forme di Acanthocerini.
Annali del Museo Civico di Storia Naturale di
Genova, 39: 450-498.
Poggi R., 2010. Gli Annali pubblicati dal Museo Civico
di Storia Naturale “Giacomo Doria” di Genova: storia
del periodico ed indici generali dei primi cento
volumi (1870-2009). Annali Museo civico Storia
naturale “Giacomo Doria”, 101: 1-530.
Wikramanayake E., Dinerstein E., Loucks C.J., Olson D.
M., Morrison J., Lamoreux J., McKnight M. &
Hedao P., 2002. Terrestrial Ecoregions of the Indo-
Pacific. A Conservation Assessment. Island Press,
Washington, 643 pp.
Biodiversity Journal, 2014, 5 (4): 525-532
Biological diversity of the National Park of El-Kala (Algeria),
valorization and protection
Sarri Djamel 1 *, Djellouli Yamna 2 & Allatou Djamel 3
'Department of Nature and life Sciences, Faculty of Science, University of M’Sila, Algeria; e-mail: djamel_sarri@yahoo.fr
2 Social science and Faculty of Arts. University of Maine, Mans. France; e-mail: Yamna.djellouli@univ-lemans.fr
department of biology, Faculty of Science.University Constantine 1, Algeria; e-mail: djalatou@yahoo.fr
‘'Corresponding author
ABSTRACT The National Park of El-Kala (PNEK, biosphere reserve) conceals a remarkable biological
and cultural richness. The investigations carried out through its territory (1996-2010) made
it possible to count 1590 vegetable species (distributed among spontaneous vascular and
introduced plants, mushrooms, lichens, algae and phytoplankton) as well as 7 1 8 animal
species. Several of these species, vegetable and animal, are protected in Algeria and belong to
the red list of the I.U.C.N. (International Union for Conservation of Nature). The safeguarding
and valorization of this richness require the installation of a management plan in adequacy
with the International Conventions of biological diversity within the framework of the durable
development, i.e. to protect and develop the natural wealth by involving residents of the
park.The aim of this paper is to present a detailed study of the flora and fauna of the entire
ecosystem of the PNEK. We insist on the considerable importance that flora and fauna bring
to the socio-economic life of the area and to its inhabitants.
KEY WORDS durable development; National Park El-Kala; natural diversity; safeguarding; valorization.
Received 13.10.2014; accepted 09.12.2014; printed 30.12.2014
INTRODUCTION
This work is an outline of a study entitled
“Durable development in the protected area of
Algeria, the case of the National Park of El-Kala
(PNEK) and the bordering areas of important eco-
logical interest”. The principal thing before any in-
tervention of valorization or protection of the
natural resources is to make a full inventory and
analysis on the biological diversity of the PNEK.
On the basis of prospection on the ground and
examination of several works and papers realized
in the area (Aouadi, 1989; Debelair, 1990; Miri,
1996; Samraoui & de Belair, 1997; Kadid, 1999;
Rezzig, 1999; Boutabia, 2000; Benyacoube &
Chabi, 2000; Sarri, 2002) and other various docu-
ments on flora of Algeria (Battandier & Trabut
1902; Maire 1952; Quezel & Santa, 1962), we tried
to inventoiy and make an assessment on the natural
richness of the PNEK, as well as a collection of the
various national and international legislative texts
which can intervene for better management and
protection of this protected surface.
The analysis of these data allowed us to make
preliminary proposals, which concern the protection
and the rational and durable use of this wealth with
national and international interest, in order to ulti-
mately pass to the phase of inquiries (Questionnar-
526
Sarri Djamel et alii
ies concerning the biodiversity and policy directives
for the durable development).
National Park of El-Kala
Located at the extreme east of Algeria, the Na-
tional Park of El-Kala extends on a surface of
76438 ha. It has some hills, not exceeding 600 m
altitude and three lakes in North, West and East
parts. The southernmost part is strewn with djebels
which culminates with djebel El-Ghorra, 1202 m
(Fig. 1).
The bioclimat is of the soft wet type with sub-
wet heat, the annual temperatures minimal average
reachs 9°C where as the annual maximum average
is 30°C. The annual precipitations average ranges
from 800 to 900 mm, often attaining a maximum of
1300 mm (Aouadi, 1989). According to Belouaham
et al. (2009), the area’s humidity of El-Kala reaches
72.4% which is relatively significant due to the prox-
imity of the littoral and the huge forests and the
whole wetlands surface, which furrow the Park ter-
ritory. Wind, usually frequent, move the dunes,
creating entirely bare spots. This is the case of the
Lake Mellah outlet and te Messida beach.
The Park is characterized by two geological for-
mations: the quaternary one, primarily represented
by marine and river deposits, with the average
Eocene corresponding to clays and sandstones of
Numidia (mainly localized in the bottoms of val-
leys), and the Miocene corresponding to conglom-
erate sands and red clays principally localized in
Southeast. The park’s grounds are those of the
forest, brown washed with a variant of forest humus
mull acid Moder. The National park of El-Kala was
created in 1983 by decree n° 83-462 of July 23rd,
1983, classified as “Reserve of the biosphere”, by
UNESCO, on December 17th, 1990.
The essential objective of the park is the protec-
tion and conservation of the floristic and faunal
components as well as of both the natural environ-
ment and cultural-historical inheritance.
Relatively less marked by the impact of human
activities, this park consists of a mosaic ecosystems
which have great biological and ecological impor-
tance. Here we distinguish:
Mediterranean Sea
Souarekh
Tl-Aioun
Souk
Ain-ELAssel
Echatt
Lac-Des
'iseaux
mm
Cheffia
Asfour
Zilouna
Chilian!
HaiiHiiam *B eni-Salali
/fBouhadjar
'ued%>» .
Tunisia
Algeria
Caption
sector of bougous
sector of brabtia
sector of oum-theboolm
limits of National Parc of El-Kala
lace and stoppings
kilometers
limits of communes
Projection UTM 31 N
Figure 1. Study area: chart of the administrative limits of the wilaya of El-Tarf (Algeria)
with the limits of the National Park of El-Kala.
Biological diversity of the National Park of El-Kala (Algeria), valorization and protection
527
- a marine ecosystem (length of 50 km), contain-
ing a particular flora and fauna (for example: red
coral) not very disrupted (varied submarine habitats
and absence of pollution).
- a dune ecosystem, consisting of a littoral dune
cord still stable (20 to 120 m of altitude), the maquis
of the kermes oak with some testifies of the floristic
procession such as: Quercus coccifera L., Juniperus
phoenicea L., J. oxycedrus L., Pistacia lentiscus L.,
Retama monosperma (L.) Boiss., Ephedra fragilis
Desf., etc...
- a lake ecosystem, constituted by the low marshy
plains and the lakes some of which are classified as
“Ramsar Sites”: lake Oubeira, (2200 ha), lake
Tonga (2600 ha), lake Mellah (860 ha, the only
lagoon in Algeria which communicates with the
sea), Marais of Bourdim (11 ha), Blue lake (3 ha)
and Black lake (6 ha).
These appreciated water tanks constitute a shel-
ter of biological richness and are of great interest
for the park habitats.
- As far as concerns the forest ecosystem, popu-
lating the mountainous zone, of average altitude,
intersected by interior depressions and dominated
by important relieves, the oak cork represents the
climactic forest on siliceous ground. It is replaced
in altitude (700 m) by the Zeen oak ( Quercus fagi-
nea Lam.).
The National Park of El-Kala is one of the most
prestigious protected zones of the Western Mediter-
ranean. It is characterized by the presence of truly
peculiar natural conditions which make it a place
of uncommon biological richness. For this reason,
it can be considereded as one of the highest relict-
ual places of the geological and biogeographical
history of the Mediterranean area (Benyacoube &
Chabi, 2000).
MATERIAL AND METHODS
This work is the result of a set of field and bib-
liographical investigations, including observation
on the field made by us, along with the follow up
of several actions, realized through the territory of
the park, joined to the consultation of several papers
(thesis, dissertation, reports, expertise, etc...) real-
ized in the territory of the park and its nearby, as
well as of all available data on the flora of Algeria
and North Africa.
RESULTS AND DISCUSSION
Floristic diversity of the National park of El-
Kala
The natural vegetation which we meet in dif-
ferent ecosystems of the National Park of El-Kala
is represented by the cork oak which dominates
with other tree species including Zeen oak,
Kermes oak, Pine of Alep, glutinous Alder,
Wilows, white Poplar, and other introduced
species as Eucalyptus , the Acacias, the Maritime
pine and the bald cypress. The floral diversity of
the national park of El-Kala is represented by 1590
botanical species. This figure includes the sponta-
neous botanical species, mushrooms, algae, lichens,
phytoplankton and the introduced or cultivated
vegetable species (Tables 1,2).
The vegetable kingdom is also rich and varied.
The lower plants (Algae, Foams, mushrooms,
Lichens) remain less studied. We count however
more than 175 (Sarri, 2006) species of mushrooms
including Truffles (560 for Algeria) and 117 species
of Lichens (Boutabia, 2000). The Higher Vascular
plants, more than 1050 species (3750 for the flora
of Algeria), were better inventoried including 382
rare and 27 protected species.
The region of El-Kala is itself a "biological cross-
roads", in time (since it reflects the succession of
the climates of Quaternary) and in space (it is char-
acterized by habitats overlap and biogeographic
interpenetrations). Species and their status are
reported in the Tables 1,2.
Biogeography of the vascular vegetable spe-
cies listed in the PNEK
Several authors (see for example: Paccalet,
1981; Ozenda, 1982; Guittonneau, 1982; Quezel,
1957, 1978, 1983, 1993; De Belair, 1995, 1996)
were interested in the study of the biogeography (of
plants and animals) considered by International
Conventions one of the criteria of appreciation of
biological diversity.
For example, Quezel (1978; 1983; 1993) re-
ported that septentrional Africa (Mediterranean and
Saharan) represents at the present time the part of
this continent where biological and ecological di-
versity is most significant (Belouahem et al., 2009)
(Figs. 3-6).
528
Sarri Djamel et alii
VEGETABLE SPECIES
STATUS OF SPECIES
N. of species
by details
N. of species
by groups
VASCULAR PLANTS
Species without status
674
1050 *
Species appearing in the red list (IUCN)
20
Protected species
27
Spontaneous medicinal species
58
Useful spontaneous species
19
Endemic species - endemic of North Africa
80
Watery and cultivated species
85
Fodder species
87
MUSHROOMS
Species without status
175
175
LICHENS
Species without status
65
117
Protected species
52
ALGAE
Species without status
70
70
THEPHYTOPLANKTON
Species without status
93
93
INTRODUCED SPECIES
Decorative introduced species
62
77
Medicinal cultivated species
15
SAILOR
Species being reported on appendices II and III of
ASP Protocol (Convention of Barcelona)
08
08
TOTAL
1590
1590
Table 1. Floristic diversity of the National Park of El-Kala, Algeria.
*: 1050 for PNEK (3750 for Algeria) including 382 rare, 122 families (128 for Algeria) and 392 kinds (907 for Algeria)
In the present study we report several plants of
different biogeographic origins (Fig. 2). In particu-
lar, the species of Mediterranean origin are most
numerous (445 species which accounts for
42.38%) followed by 5.24% of species of tropical
origin which shows the first origin of the site. The
specific biological diversity observed wihin the
National park of El-Kala (which belongs to Alge-
rian Numidia) is related to the favorable ecological
conditions which allow the preservation of these
species.
In fact, in sub-littoral Numidia both the high
temperatures in summer and the accentuate humid-
ity, due to the dune barrier, combine together to
create a real subtropical climate. On the other hand,
wintry weather conditions (low T°C and high plu-
viometry) contribute to create a remarkable mode-
rate climate (Belouahem et al., 2009).
Note. The presence of the two protected vascu-
lar plants Euphorbia dendroies L. and Orchis
provincialis Balbis is uncertain;
- the truffle Terfezia arenaria (Moris) Trappe
(1971), reported in the littoral dunes of the territory
of the park, represents some sort of curiosity;
- the very few studies on the flora in this region
make our study very difficult;
- the document on flora of Algeria should be up-
dated as based on data by Quezel & Santa (1962-63);
- floristic list may change at any time due to the
large area and its ecological characteristics.
Fauna diversity of the National park of El-
Kala
The most important groups of animals we ob-
served in the National Park of El-Kala include
Biological diversity of the National Park of El-Kala (Algeria), valorization and protection
529
Subdivisions
biogeographic
Numbers by geo-
graphical category
Percentage
Mediterranean
species
445
42.38
Species of
transitions
280
26.66
Scandinavian
species
125
11.90
Endemic species
75
7.14
Cosmopolitan
species
64
6.10
Tropical species
55
5.24
Species without
indications
6
0.57
11,6
Scandinavian
42.66
Mediterranean
5.24 Tropical
6.1 Cosmopolitan
7.14 Endemic
0.6 without inication
26.66 transition
Table 2. Frequencies and number of species inventoried in
the PNEK by biogeographic subdivisions.
Figure 2. Biogeographic spectrum of the National
Park of El-Kala, Algeria (expressed in %).
Figure 3. Geranium atlanticum B.R., endemic ofN-Africa. Figure 4. Scolopendrium vulgare Sm., very rare species.
Figures 5, 6. Campanula alata Desf., endemic of Algeria-Tunisia, Red List-IUCN.
mammals, insects, reptiles, Amphibians, birds and
fish. We counted up to 706 animal species includ-
ing the zooplankton (Table 3). The National Park
of El-Kala is one of the last refuges for the stag
endemic to Algeria and Tunisia. Forty years ago,
there were more than 300 individuals. This number
fell considerably because of the hunting and the
forest fires. Currently, its number does not reach
30 individuals; maybe less. Several animal species
are endemic to the region, others are more widely
distributed, but they do not live any more in the
area. The faunistic list can change at any moment
seen the importance of the zone for its surface and
ecology (Figs. 7-9).
Protection and valorization of the richness
The years lived in the National Park of El-Kala,
allowed us to gather information about the needs
and the socio-economic activities of the inhabitants
as well as a considerable knowledge on its natural
and even cultural potential.
Rational and durable exploitation of the flora
Several examples can be enumerate:
- the cork oak for its cork;
- heathers for the clothes industry of pipes and
ornament;
530
Sarri Djamel et alii
- fruit trees of forest (Olive-tree, Cane-apple
bush, Myrtle, Hawthorn. . .) for food purposes;
- the medicinal plants (Bay-tree sauce, Laven-
der, Myrtle...) have great potentials (they can be
employed directly, i.e. roots, leaves, flowers, or by
extraction of essential oils and/or substances to be
used for pharmaceutical products);
- decorative plants (including ferns, and many
Liliaceae;
- mushrooms (including truffles) for food pur-
poses;
- olive oil and mastic tree oil.
All plants quoted above can become an impor-
tant source of incomes for the residents (inhabitants
of the park) and thereafter for the investors.
Within the framework of the valorization of the
flora, we also record the various scientific works in
phytochemistry done by national researchers, which
one of the Authors participated to by collecting and
identifying several samples: Genista aspalathoides
Lamk ssp. erinaceoides (Lois.) Maire, Genista
ferox Poirret, Genista ulicina Spach, Genista tricus-
pidata Desf., Serratula cichoracea (L.) DC., Hal-
imium halimifolium (L.) Willk., Matricaria
chamomilla L., etc...
The idea is to create small eco-exploitation
farms or eco-companies which cultivate, protect,
exploit, and trade local products (at the finished or
raw state) in a rational and long-lasting way through
their own territory (in the short and medium term)
and, in the future, towards abroad (in the long term).
Rational and durable exploitation of fauna
Among the animal species occurring within the
Park, the least protected and valued are water birds,
sea and freshwater fish (as the eel), mollusks (as the
clam of the Melah lake) and the deer ( Cervus ela-
phus barbarus Bennett, 1833). The extraction of the
Coral requires some precautions because it is in per-
manent reduction. To avoid the disappearance of the
stag from the National Park of El-Kala and even
from the whole Algeria, a program was set up for
breeding it in captivity and in a so-called “bilateral”
semi-captivity, between the National Park and the
hunting center of Zeralda, with the aim of ensuring
its existence, perenniality and releasing them peri-
odically. Until 2002 it produced more than 50 indi-
viduals.
These results, which are very satisfactory and
encouraging, let us think and suggest that, altough
it ensures a good protection of this animal, with a
rigorous application of legislative texts and the mul-
ANIMAL SPECIES
NUMBER OF SPECIES
OTHER DETAILS
PROTECTED
SPECIES
MAMMALS
43
(107 for Algeria in [6])
Terrestrial 39
Sailors 04
17
REPTILES
ET AMPHIBIANS
24 (82 for Algeria)
Reptiles 19
Amphibians 05
03
INSECTS
215
All groups 215
13
BIRDS NICHOR
AND MIGRATING
214
(402 for Algeria in [16])
water and forest birds 1 1 7
birds navy 12
Raptors 25
26 and 3 1
02
25
FISH
128
marine fish 104
fresh water fish 24
09
ZOOPLANKTON
94
Mollusques (clams) 55
Crustacees (crustaceans) 33
Brachinopodes (brachiopods) 03
Tuniciens (tunicates) 03
TOTAL
718
718
126
Table 3. Faunal diversity of the National Park of El-Kala, Algeria.
Biological diversity of the National Park of El-Kala (Algeria), valorization and protection
531
tiplication of breeding programs, in a short time we
could get to the point where we could see the meat
of the stag for sale from the butcher. Meat which,
in turn, would come from regular regulated and
paying hunting tourism.
Or, still, one can quote another economic activ-
ity practised in the territory of the park representing
a good source of job and currency, i.e., the har-
vesting of snails, which are generally sold at 200
DA for kilo to Tunisians.
The legislative arsenal protecting national parks
(protected areas)
A collection of 133 legislative texts was carried
out. This arsenal of texts reflects the importance of
the national natural inheritance of the national park
of El-Kala. These texts give a great support to the
management of the whole protected area of the
Country. In reality, these laws are constantly disre-
garded (are not met) and do not give any real indi-
cation neither to managers nor to administrations
and residents.
CONCLUSION
The originality of the National Park of El-Kala
returns especially to its biological diversity. A floris-
tic diversity of 1590 vegetable species including
1050 vascular seedlings (27 protected, 80 endemic
and 20 species appearing in the red list (IUCN)),
175 mushrooms, 117 lichens (52 protected), 70
algae, 93 species of phytoplankton, 77 species of
vascular introduced and cultivated plants as well as
eight vegetable sailors species being reported on
Appendix II and III of Protocol of the Convention
of Barcelona.
The faunal diversity is marked by 7 1 8 animal
species including 43 species of mammals (17 pro-
tected), 24 reptiles (3 protected) and Amphibians,
215 insects (13 protected), 214 species of birds
(87 protected), 104 marine fish species (9 protected),
24 fresh water fish species and 92 species of zoo-
plankton. To preserve this originality, the study rec-
ommends creating small Eco-exploitations farms or
eco-companies, which exploit and at the same time
protect this floristic and faunistic richness. One
should not forget that the flora and fauna not only
represent an important source of incomes for the in-
Figure 7. Delicious Lactaire; possibility of potential signifi-
cant culture. Figure 8. Exploitation of light for drying of the
cork. Figure 9. The Barbary stag in semi captivity.
habitants of the park but also can contribute to in the
economic development of country. The knowledge
of faunistic and floristic diversity and of the distri-
bution methods of the fauna and flora of a territory,
532
Sarri Djamel et alii
allows us to have an effective tool for control and
management of the natural habitats.
It is up to people having in charge and managing
the protected areas, and a good information helps
in directing reasoned actions of maintenance of the
Territory. The park of El-Kala is a national heritage.
Unfortunately, today we are witnessing a series of
irresponsible and irrational behaviors that demon-
strate a lack of education and environmental aware-
ness. It is important that people understand that the
peculiarities of PNEK reflect the deep meaning of
Numidia and Krumiria (Northeast Algeria) and
therefore this park is a treasure that must be pro-
tected and defended.
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Biodiversity Journal, 2014, 5 (4): 533-544
Sloth bear, Melursus ursinus Shaw, 1 79 1 (Mammalia Ursidae),
from India: conservation issues and management actions, a
case study
Vikas Kumar 1 *, AmitA. Revale 2 , Sachin K. Singh 2 , Maulik Amlani 2 & Abduladil A. Kazi 2
'College of Forestry, Kerala Agricultural University, Thrissur, Kerala - 680656 India
2 ACHF, Navsari Agricultural University, Navsari, Gujarat - 396450 India
■"Corresponding author, email: vkskumar49@gmail.com
ABSTRACT One of the 12 mega biodiversity centres of the world, India is unique in having four of the
eight bear species (Mammalia Ursidae) that are found in the world. They are brown bear
( Ursus arctos Linnaeus, 1758 s.L), Asiatic black bear ( Ursus thibetanus Cuvier, 1823), sun
bear ( Helarctos malayanus Raffles, 1821) and sloth bear (. Melursus ursinus Shaw, 1791). The
abundance of sloth bear in India, which is also present in Sry Lanka with the endemic sub-
species Sri Lankan sloth bear, M. ursinus inornatus Pucheran, 1855, is determined by its
location within the global distribution range, quantum, quality and continuity of habitat
available and the anthropogenic pressures the species faces. Bears in India are threatened due
to poaching for bear parts, retaliatory killings to reduce conflicts and habitat loss due to
degradation and fragmentation. In addition to these concerns, the rehabilitation of communi-
ties that eke out a living on dancing bears has made bear conservation a challenge in India.
Deforestation and hunting are major threats to bears in India. Unless urgent conservation mea-
sures are taken and degraded forest areas are restored, we suspect that sloth bear may soon
become endangered in India.
KEY WORDS Bear-human interactions; conservation; habitat; management; sloth bear.
Received 15.10.2014; accepted 11.12.2014; printed 30.12.2014
INTRODUCTION
In the world, there are about 5,416 species of
mammals distributed in about 1,229 genera, 153 fam-
ilies and 29 orders (Wilson & Reeder, 2005). Four
hundred and twenty species of mammals (7.75 %
of the world’s mammals) are known from India
(Nameer, 2008). Among the mammals carnivores
are the most widely distributed terrestrial animals
on earth (Schipper et al., 2008). Bears are mammals
that belong to the family Ursidae G. Fischer de Wald-
heim, 1817 and represented by seven living species
that are widely distributed in a variety of habitats
throughout the Northern Hemisphere (Table 1).
Bears are found on the continents of North America,
South America, Europe and Asia. Out of seven
known species of bears, five are seen in India which
includes Himalayan brown bear, Himalayan black
bear, Malayan sun bear, brown bear and sloth bear.
Common characteristics of modem bears include a
large body with stocky legs, a long snout, shaggy
hair, plantigrade paws with five non-retractile claws
and a short tail. The lips are free from the gums and
protrusible. Bears rely principally on their sense of
534
Vikas Kumar et alii
No.
Scientific name
Common
name
Status
1 .
Ursus americanus
Pallas, 1780
American
black bear
Least
concern
2.
Ursus arctos
Linnaeus, 1758
Brown bear
Endangered
3.
Ursus thibetanus
Cuvier, 1823
Asiatic black
bear
Vulnerable
4.
Helarctos malaya-
nus Raffles, 1 82 1
Sun bear
Vulnerable
5.
Melursus ursinus
Shaw, 1791
Sloth bear
Vulnerable
6.
Ursus maritimus
Phipps, 1774
Polar bear
Vulnerable
7.
Tremarctos orna-
tus (Cuvier, 1825)
Spectacled
bear
Vulnerable
Table 1 . Seven species of bears in the world
(Sourse: I.U.C.N., 2012).
smell however the eye sight and hearing are com-
paratively poor (Prater, 1971). Bears are placed in
the order Carnivores but, except for the largely car-
nivorous polar bear, bears are omnivorous, feeding
mostly on plant material, insects, fish, and mam-
mals. They are generally large, stocky, and powerful
animals. All bears are plantigrade, walking on their
entire foot. Their activities are mainly governed by
the availability of food items and directly compo-
nents within their habitat (Joshi et al., 1999b).
Sloth bear ( Melursus ursinus ) is one of the four
bear species found in India and is entirely tropical
in distribution and posses several morphological,
physiological and behavioural adoptions to the trop-
ical habitat. Most sloth bears are found in India and
Sri Lanka (in this island with the endemic sub-
species inornatus Pucheran, 1855, Sri Lankan sloth
bear) but they have also been reported from
Bangladesh, Nepal and Bhutan (Garshelis et al.,
1999a; Johnsingh, 2003; see also http://www.
bearbiology. com). In India, sloth bears are found
from the foothills of Himalayans to the Southern
end of Western Ghats (Yoganand et al., 2006). They
are also found in the Brahmaputra Valley of Assam
(Cowan, 1972; Krishnan, 1972; Brander, 1982). It
may still occur in the wet forest regions of eastern
Bangladesh (Khan, 1982; Servheen, 1990) border-
ing the Mizoram state of India, from where it has
been reported (Yoganand et al., 1999). They appar-
ently favour drier forests and have been reported to
prefer areas with rocky outcrops. In India, 90% of
sloth bear populations are confined in the dry and
moist deciduous forests of which the former
account for 50% of the sloth bear populations. Sloth
bear also occur in tropical evergreen forests, scrub
lands and rocky hills. The bear lives in a variety of
habitat such as Teak forest and Sal forest, lowland
evergreen forest and the hill countiy up to elevation
of 1700 m and riparian forests and tall grass areas
on the floodplains of Nepal (Joshi et al., 1997).
However, their relative abundance varies across
these vegetation types, as indicated by their higher
abundance in deciduous forests, followed by dry
deciduous, scrub and evergreen forests. Recent
local extirpations and population declines have also
been reported from the north-western populations
(in the state of Rajasthan), a few isolated forests in
the northern Western Ghats and adjoining areas,
along the north-western Shivalik hills (no recent
record of sloth bears to the west of the river
Ganga), the northern forested areas of the state of
West Bengal bordering Sikkim and Bhutan, and in
the north-eastern states of India (Yoganand et al.,
1999). To suit the tropics, it has no underfur;
however, it has a long coat that perhaps helps in
defending it from insect bites and also perhaps to
exaggerate its size to predators (such as tiger and
leopard) or conspecifics.
The sloth bear’s low metabolic rate and high
thermal conductance (McNab, 1992) may be advan-
tageous in the hot climates where it lives, in that it
reduces heat production and facilitates heat loss.
Sloth bears seem to also have a behavioural adap-
tation to avoid hot weather conditions in their
habitat by reducing daytime activity.
Clutton-Brock & Harvey (1983) suggested as
advantages of having large body size, we speculate
that the large body size of the sloth bear might help
it to conserve heat; to travel great distances in
search of its dispersed, seasonal food; to enhance
the ability to survive on qualitatively poorer food
of insects and fruits; to enable it to break hard ter-
mite mounds and to dig deep into social insect
colonies; or to help it store fat and live on it during
periods of shortage and during parturition denning.
The potential sloth bear distribution range in India
was estimated to be about 200,000 Km 2 (Johnsingh,
Sloth bear, Melursus ursinus (Mammalia Ursidae), from India: conservation issues and management actions, a case study 535
2003; Akhtar, 2004; Chauhan, 2006). But the recent
surveys indicate the distribution range to be
400,000 Km 2 .
Sloth bear is small bear with a shaggy coat espe-
cially over the shoulders with grey and brown hairs
mixed in with the dark black coat. It has a distinc-
tive whitish or yellowish chest patch in the shape
of a wide U, or sometimes a Y if the lower part of
the white hairs extends down the chest. The snout
is light coloured and mobile. It is thought that the
reduced hair on the muzzle may be an adaptation
for coping with the defensive secretions of termites.
Adult males weight 80-140 Kg and females weight
55-95 Kg (Prater, 1980; Garshelis et al., 1999b).
Physical adaptations for digging and eating insects
include long, slightly curved claws, a broad palate
for sucking, the absence of two front upper incisors
and large protmsible lips (Harris & Steudel, 1997).
Its vernacular name is bhalu (Hindi), Karadi (Tamil
and Malayalam). Mating generally takes place be-
tween May and July and the cubs are bom between
November and January (Jacobi, 1975; Laurie &
Seidensticker 1977; Joshi et al., 1999b).
The actual period of pregnancy is shorter, as the
fertilised egg is implanted after a period of delay
(Puschmann et al., 1977). Similar to what is ob-
served in the temperate bear species. In captivity,
mating pairs come together for only one or two days
during which time there may be considerable vocal-
izing and fighting. Gestation lasts from six to seven
months. Most litters consist of either one or two
cubs, but litters of three cubs have been reported.
Cubs are bom in earth dens and apparently do not
leave them until they are two to three months old.
The cubs stay with their mothers who carry them
on their backs until they are nearly two or more
years of age (Joshi et al., 1999b).
Bears are usually solitary with the exception of
courting individuals and mothers with their cubs.
They are generally diurnal, but may also be crepus-
cular or nocturnal, particularly in and around human
habitations. Bears have excellent sense of small and
are good climbers and swimmers. Many bears of
northern regions go into a period of dormancy dur-
ing winters colloquially called hibernation. Sloth
bears are one of the largest termite-eater among
mammals. A significant portion of then diet consists
of ants and termites (Schaller, 1969; Eisenberg &
Lockhart, 1972; Laurie & Seidensticker, 1977;
Joshi et al., 1999a) and hence the sloth bear is con-
sidered as the only myrmecophagous among Ursi-
dae. Since some Ursids disperse seeds they are con-
sidered to be important seed dispersers for many
tropical plant species where fruits form major part
of their diet (Baskaran, 1990; Willson, 1993; Parley
& Robbins, 1995; Welch et al., 1997; Auger et al.,
2002; Kitamura et al., 2002; Sreekumar & Balakr-
ishnan, 2002; Koike et al., 2008). Around the world,
bears and humans have co-existed for centuries as
evident from the references of bears in ancient art,
culture, folklore, epics, religion and literature. Bears
are good indicators of habitat quality as they occupy
the position of an apex predator in a few ecosys-
tems. They are unique in the sense that they could
feed on plants, prey on other species as well as scav-
enge dead animals.
Sloth bears feed extensively on termites and have
special adaptations for doing this. The naked lips are
capable of protruding and the inner pair of upper
incisors is missing and the inner pair of lower in-
cisors is missing, which forms a gap through which
termites can be sucked. The sucking noises made by
feeding in this manner can apparently be heard from
over 100 meters away. They also eat eggs, other
insects, honey combs, carrion and various kinds of
vegetation including fruits (Gokula et al., 1995;
Joshi et al., 1997). The sloth bears consume plant
species included Cassia fistula L., Zizyphus oenoplia
(L.) Mill., Glycosmis pentaphylla (Retz.) DC.,
Holigarna arnottiana Wall, ex Hook, f., Fins spp.,
Syzygium cumini (L.) Skeels., Grewia tilifolia Vahl,
Mangifera indicaL., Bridelia retusa (L.) A. Juss. and
Cardia dichotoma G.Porst. (Sajeev, 2013).
As a result of the continued habitat destruction
and degradation, sloth bear populations have de-
clined or become fragmented all over and as a
result, they have become locally extirpated in some
areas (Cowan, 1972; Krishnan, 1972; Servheen,
1990; Murthy & Sanlcar, 1995; Garshelis et al.,
1999a; Singh 2001; Johnsing, 2003). Sloth bear is
included in Schedule I of India Wildlife Protection
Act- 1972 and Appendix I of the Convention on In-
ternational Trade in Endangered Species of Wild
Elora and Fauna (C.I.T.E.S.).
POPULATION STATUS AND HABITAT
The Central Zoo Authority (C.Z.A.) is statuary
Ministry of Environment & Forests, Government of
536
Vikas Kumar et alii
India established in 1992 to oversee the functioning
of zoos in India and provide technical assistance.
There are 70 Zoos and five Rescue Centers housing
a total number of 795 individual (as on 3 1st March,
2012) bears in captivity for the purpose of conser-
vation, education to the public and for their lifetime
care (Table 2). The distribution and details of the
bear species housed in various Indian Zoos & Re-
scue Centers are shown in figure 1 and Table 3.
CONSERVATION ISSUES
I. Threats to the species
Sloth bear is protected by inclusion in Schedule
1 of the wildlife (Protection) Act 1972. The sloth
bear population in India is threatened largely by
poaching (Garshelis et al., 1999b). Bears have been
poached for gall bladder and other parts, which are
often exported to South-East Asian countries as an
ingredient to Traditional Chinese Medicines. In the
last five years, poaching and hunting has become
uncommon as reported by the Government of India.
Incidence of sloth bears getting killed by road and
railway hits and electrocution were also noted. In
Odisha, based on only the recorded cases by the
forest department, the total number of sloth bears
killed is over 30 in last five years.
A number of sloth bears (n=8) died in the state
due to road and train accidents in last five years as
recorded by the forest department. It is also reported
that the bears might be poached/hunted in some
areas but access to these areas is limited due to se-
curity issues. Trade of live bear cub and bear body
parts poses a direct threat to the animal and its
future survival in the state. With adjoining state like
Chhattisgarh, Maharashtra and Odisha reporting
presence of illegal trade routes, the trade is likely
to exist in Madhya Pradesh as well. Sidhi, Shivpuri
and Shahdol districts of Madhya Pradesh are con-
sidered sloth bear cub poaching hot spots. The rea-
sons for the lack of information on illegal trade can
be attributed to:
a. Infrequent poaching of sloth bears in the
region.
b. Strong networking among the defaulters that
help them got by unnoticed by the authorities.
c. Because reporting poaching is considered a
disgrace.
The sloth bear has the most widely recorded
SL. No.
Species of Bear
Male
Female
Un-
known
Sex
Total
No. in
Zoos
No. on
Rescue
Centers
No. of
Zoos
No. of
Rescue
Centers
1
Sloth bear
Melursus ur sinus ur sinus
Shaw, 1791
292
267
3
562
251
311
40
3
2
Himalayan black bear
Ursus thibetanus laniger
(Pocock, 1932)
106
95
22
223
211
12
53
2
3
Himalayan brown bear
Ursus arctos isabellinus
Horsfield, 1826
3
1
1
5
5
0
1
0
4
Malayan sun bear
Helarctos ma lay anus
malayanus Raffles, 1821
1
3
0
4
4
0
2
0
5
European brown bear
Ursus arctos arctos
Linnaeus, 1758
1
0
0
1
1
0
1
1
TOTAL
403
366
26
795
472
323
97 (70)
6(5)
Table 2. Statuses of bears in Indian Zoos (as on 31st March, 2012).
Sloth bear, Melursus ursinus (Mammalia Ursidae), from India: conservation issues and management actions, a case study 537
distribution range than any of large carnivore in
Central India (Jhala et al., 2011). The erstwhile state
of Madhya Pradesh (undivided Madhya Pradesh in-
cluding Chhattisgarh) had largest sloth bear popu-
lation in this country with the bear inhabiting an
area of 135,395 Km 2 of the forest (Rajpurohit &
Krausman, 2000).
In Central India, sloth bear is locally considered
as one of the most feared and dangerous wild ani-
mals (Bargali et al., 2005). Sloth bear seem to have
a very low tolerance toward humans. Majority of
the HBC cases have occurred either when the
human enters sloth bear habitat or when the sloth
bear enters kitchen gardens in the village home-
steades. Maximum conflict cases have occurred in
the month of March and early April, which coin-
cides with Mahua, Madhuca indica (J. Konig) J.F.
Macbr., season when both bears and human com-
pete for the same resource. The conflict intensity
may raise up to 2.23 cases per day during this
period, while in other months; it comes down to 1 .4
cases/day (Sarkar, 2006).
In Maharashtra, however, bear-human conflict
especially in district of Chandrapur, Gondia, Gad-
chiroli, Bhabdara, Akola and Amravati in the Vi-
darbha region is on the rise. In Tamil Nadu, only
one poaching case was recorded across the state dur-
ing the past five years in Gudalur Forest Division.
Apart from this, two more bears were killed possi-
bly due to conflict in 20 1 0-20 1 1 . A total of 20 cases
of conflict have been recorded in the state in the last
five years (2006-2011) including 19 cases of human
injuries and one case of human death. However,
much information on human-bear conflict is lacking
from this state.
Other edibles valued by bear as well as humans
are Jamun, Syzygium cumini (L.) Skeels., Bair,
Zizyphus spp., Tendu, Diospyros melanoxylon
Roxb, Bel, Aegle marmalos, (L.) Correa, Chironji,
Buchanania lanzan Spreng., and honey. Therefore,
when both human and bear share the same space
and depend on the same resources, the conflict
(human injuries and human death) becomes in-
evitable. Because of such negative interaction,
attrition levels among the locals rise, often leading
to considerable number of bears being persecuted
and killed in retaliation. No poaching of bear or
incident of trade in bear or bear parts has been
recorded by the forest department of Gujarat in
last five years.
II. Threats to the habitats
Implementation of Schedules Tribes and Forests
Dwellers Act, 2006 will also have an impact on bear
converted into arable land. Change in cropping pat-
tern is also harming the bear food availability in the
area. Due to fragmentation of forests, sloth bears
often enter villages to ride agriculture and forage
on wild ficus and horticultural produce being
processed (Mango, Anona, Mahua, Ground nut,
Maize and Sweet potato). Some villagers are now
resorting to alternate crops that do not attract bears.
Large source of bear food is being removed from
around villages intentionally which ultimately will
have a bearing on sloth bear population in Chhat-
tisgarh (Akhtar et al., 2006a).
Outside the protected areas, sloth bear habitat in
territorial forest divisions is facing habitat degrada-
tion due to various activities including anthropolog-
ical pressures from local communities, quarrying of
granite and sandstone, diversion of forest land for
non-forestry purposes and illegal cultivation by
local communities. Due to habitat fragmentation,
Sloth bear populations are getting encircled by agri-
culture activity around foothills of hillocks whereby
they get confined to hill portions like in Jaffarghat
Fort and Warangal District in Andhra Pradesh. The
sloth bear habitat between India and Nepal is con-
nected through northern Bihar (Terai Arc Land-
scape) and the sloth bear population in central and
eastern Indian landscape are connected through
southern Bihar. These sloth bear occupied areas
under threat due to various anthropogenic reasons,
which needs special management emphasis (Gupta
et al., 2007).
The potential sloth bear habitat range in Amnachal
Pradesh is about 1500 Km 2 . Here, sloth bear habitat
is threatened due to slash and bum or jhum cultiva-
tion, deforestation and encroachment. Construction
of roads and infrastructure development, tea plan-
tation and development of human settlements in
foothills and adjacent plains have also threatened
the potential sloth bear habitat, leading to habitat
loss and degradation (Choudhury, 2011).
The sloth bear habitat in Gujarat mostly occurs
in terminating mountain ranges of Arawalis, Sapuda
and Sahiyadri with dry deciduous to moist forest
types. Fmits and other parts of more than 35 plant
species have been reported from here, which is are
consumed by sloth bears (Mewada, 2011).
538
Vikas Kumar et alii
Figure 1. Sloth bear, Melursus ursinus ursinus, distribution in India.
The main issues with the available bear habitat
in the state are pressure on the habitats by livestock
grazing, tourism and developmental activities and
mining, which are reported as major factors leading
to habitat degradation and fragmentation of forest
patches. Out of seven forest divisions with sloth
bear population in this state, forest patches in four
divisions are unprotected and not declared as
sanctuaries.
MANAGEMENT ACTION
Stakeholder involvement in various aspects of
wildlife management can yield many benefits
(Chase et al., 2000). The specific conservation
recommendations for minimizing bear-human con-
flicts and bear habitat conservation are as fol-
lowing.
I. Protection to the species
The sloth bear is listed in Schedule I of the
Indian Wild Life (Protection) Act (Govt, of India,
1972; Govt, of India, 2003), Vulnerable (I.U.C.N.,
2012). Special powers accorded to the forest staff
in Assam have enabled them to patrol the protected
areas more effectively than other parts of the coun-
try. However, in areas outside the protected areas,
lack of and inadequately trained staff hampers
protection measures.
There is no specific strategy for protection of
sloth bear in Bihar (Govt, of Bihar, 2012), Haryana
and Gujarat. However, being found in the protected
areas of the state, the species gets the highest
degree of legal safeguard. Lack of reliable infor-
mation network restricts intelligence-based en-
forcement to control poaching and illegal trade.
Majority of bear habitats fall outside the jurisdic-
Sloth bear, Melursus ursinus (Mammalia Ursidae), from India: conservation issues and management actions, a case study 539
tion of protected area network of the state, they
lack protection equipments, trained man power and
local rescue team. In Andhra Pradesh, the sloth
bear is listed in Vulnerable (A2 cd+4cd; Cl) cate-
gory of I.U.C.N. Red List of threatened species
(Garshelis et al., 2008).
II. Habitat management
The development projects such as roads, irriga-
tion dams, hydro-electric project in the wildlife
sanctuaries are the major threats to bear habitat in
the state of Kerala, Tamil Nadu and Karnataka. The
impact of such developmental activities on sloth
bear status and distribution is not known and often
is ignored. In Gujarat, forest field staffs manage
habitats in almost all the forest divisions, which
include regular monitoring, plantation programs,
often with committee’s involvement. Eco develop-
ment committees, village development committees,
stakeholders groups are formed in each forest divi-
sion to carry out habitat restoration and improve-
ment programs. Community forestry programs,
wherein local people learn the value of planting and
protecting trees, could expand habitat for sloth
bears, and could also reduce the bear-human
interactions. The strength of this approach is that it
is instigated from the bottom up (i.e., people do it
because it benefits them, rather than because it is
mandated), but it also must be supported from the
top down (Poffenberger, 1990).
III. Management of bear-human interactions
No specific management actions have been
taken for sloth bear human interaction in many of
the states such as Arunachal Pradesh, Assam, Bihar,
Jharkhand, Gujarat, Rajasthan, Meghalaya, Naga-
land and Uttrakhand. In Chhattisgarh, there is a
policy for compensation by financial reimburse-
ment in case of human mauling or killing by wild
animals but not for crop depredation; in Mahara-
shtra, Madhya Pradesh, Uttar Pradesh, West Bengal
and Goa state there is a policy for ex-gratia for crop
damage or human causalities due to bear of Rs
1,00,000/-, and up to Rs 75,000/- for permanent dis-
ability due to bear attacks. In addition to the reim-
bursement of medical expenses, forest department
also provides compensation for the loss of man days
incurred by the victim as a welfare scheme.
In Maharashtra, sloth bear is known for its ag-
gressiveness, both towards humans and towards
other large mammals. The survey conducted by
Wildlife Trust of India indicates that between 2006
to 201 1, Gondia has reported the maximum number
of human sloth bear conflict cases (65) followed by
Chadrapur (36) and Bhandara (26). Desai et al.
(1997) reported that bear-human interactions are
very common issue in all districts of Gujarat except
Panchmahal district. The Gujarat states recorded
127 human sloth bear interaction cases in the last
five years, of which 95 were cases of human in-
juries with one casualty (Mewada, 2011). Se-
shamani & Satyanarayan (1997) have reported that
Jharkhand has a long history of the human-bear
conflict but the State does not have effective strat-
egy to deal with the human-bear conflict. According
to Karnataka Forest Department records, the bear-
human conflicts are severe in five districts namely
Chamrajnagar, Chickmagalur, Tumkur (maximum),
Chitradurga and Bellary. In Kerala the forest depart-
ment has provided proper guidance to villagers liv-
ing aroung bear-bearing areas such as Periyar Tiger
Reserve and Parambikulam Tiger Reserve on how
to avoid interaction with sloth bear. The question-
naire survey results shows that in only five out of
34 forest divisions recorded sloth bear-human con-
flict namely Kannur, Wayanad, Palghat, Emakulam
and Kollam. Incident of poaching, confiscation and
retaliatory killings seem to be few in the Odisha and
Tamil Nadu states (Baslcaran et al., 1997). Other
measures to mitigate human bear conflict include
promotion of awareness through various awareness
programmes and hoarding on sloth bear conserva-
tion. In addition in few states forest departments
have provided drums and crackers to villagers to
chase bears away from villages. Andhra Pradesh
Forest Department has made a provision to have a
Conflict Management Team at the Circle level. In
the recent years remote drug delivery devices (tran-
quilizing equipments) have been purchased in
Valmiki Tiger Reserve (Govt, of Bihar).
IV. Research and Information
Scientific information on sloth bear is restricted
to a few status surveys, conflict surveys and short
studies (Gopal, 1991; Johnsingh, 2003; Chauhan &
Rajpurohit, 2006; Dharaiya & Ratnayeke, 2009;
Dharaiya, 2010; Choudhury, 2011).
540
Vikas Kumar et alii
SL.
NO.
ZOO NAME
MALE
FEMALE
UNSEX
TOTAL
1
Agra Bear Rescue Facility, Agra
139
129
0
268
2
Alipore Zoological Garden, Kolkata
1
2
0
3
3
Amtes Animal Ark, Wardha
1
2
0
3
4
Arignar Anna Zoological Park, Vandalur,
Chennai
4
4
0
8
5
Aurangabad Municipal Zoo, Aurangabad
1
1
0
2
6
Bhagwan Birsa Biological Park, Ranchi
5
3
0
8
7
Bondla Zoo, Usgao
2
2
0
4
8
Children Park & Zoo, Gadag
1
0
0
1
9
Dr. K. Shivarma Karanth Pililcula
Biological Park, Mangalore
0
1
0
1
10
Dr. Shyamaprasad Mukharjee Zoological
Garden, Surat
2
2
0
4
11
Gandhi Zoological Park, Gwalior
0
1
0
1
12
Indira Gandhi Park Zoo, Rourkela
1
1
0
2
13
Indira Gandhi Zoological Park,
Visakhapatnam
2
6
0
8
14
Indira Priyadarshini Sangrahalaya,
Anagodu, Davangere Taluk
0
1
0
1
15
Jaipur Zoo, Jaipur
3
1
0
4
16
Jhargram Zoo, Jhargram
0
4
0
4
17
Kamla Nehru Prani Sanghrahalaya Zoo,
Indore
1
1
0
2
18
Kamla Nehru Zoological Garden,
Ahmedabad
1
0
0
1
19
Kanan Pandari Zoo, Bilaspur
4
3
0
7
20
Kanpur Zoological Park, Kanpur
1
1
0
2
21
Karuna Society For Animals and Nature-
Rescue Centre, Dist. Anantapuram
2
2
0
4
22
Lucknow zoological Park, Lucknow
1
2
3
23
Maharajbag Zoo, Nagpur
1
1
0
2
24
Mahendra Chaudhury Zoological Park,
Chhatbir, Chandigarh
3
2
0
5
25
Maitri Baagh Zoo, Bhilai
2
1
0
3
26
Mini Zoo A. M. Gudi Balvana,
Chitradurga
0
2
0
2
27
Nandankanan Biological Park,
Bhubaneshwar
4
3
0
7
28
National Park, Bannerghatta Zoological
Garden, Bangalore
59
45
0
104
Table 3. Records of sloth bear, Melursus ursinus ursinus, in India zoos (continued).
Sloth bear, Melursus ursinus (Mammalia Ursidae), from India: conservation issues and management actions, a case study 541
SL.
NO.
ZOO NAME
MALE
FEMALE
UNSEX
TOTAL
29
National Zoological Park, Delhi
2
2
0
4
30
Nehru Zoological Park, Hyderabad
5
4
0
9
31
Pt. Govind Ballabh Pant High
Altitude Zoo, Nainital
0
0
0
0
32
Rajiv Gandhi Zoological Park and
Wildlife Research Center, Pune
3
1
0
4
33
Ramnabagan Mini Zoo, Burdwan
1
1
0
2
34
Sakkarbaug Zoo, Junagarh
3
2
0
5
35
Sanjay Gandhi Biological Park, Patna
4
2
0
6
36
Sri Chamarajendra Zoological
Gardens, Mysore
5
5
0
10
37
Sri Venkateswara Zoological Park,
Tirupati
3
2
0
5
38
Tata Steel Zoological Park, Jamshedpur
1
2
0
3
39
Thiruvananthapuram Zoo,
Thiruvananthapuram
1
1
1
3
40
Tiger & Lion Safari, Shimoga
1
1
0
2
41
Van Vihar National Park, Bhopal
19
17
0
36
42
Vanavigyan Kendra, Hunter Road,
Hanamkonda, Warangal
1
1
2
4
43
Wild Animal Conservation Centre,
Mothijharan, Sambalpur
2
3
0
5
TOTAL
292
267
3
562
Table 3 (continued). Records of sloth bear, Melursus ursinus ursinus, in India zoos.
A few intensive studies on sloth bear ecology
were carried out in Panna National Parks (Yo-
ganand et al., 2005) and North Bilaspur Forest Di-
vision (Akhtar & Chauhan, 2000; Akhtar, 2004;
Bargali, 2004; Akhtar, 2006; Akhtar et al., 2008;
Mewada, 2011). However, there is lack of even
basic information on sloth bear presence/ absence
for many areas in North-Eastern states. Information
on population estimates, relative abundance and
monitoring are wanting.
V. Capacity Building
Apart from some wildlife managers and front-
line staff, most of the field managers and staff
require capacity building. Other stakeholders
require sensitization and training in order to help
protection on sloth bear, its habitat and reducing
sloth bear-human conflict.
VI. Awareness Campaign
The majority of the local people are uneducated
as they are primitive tribes of the region and still at-
tached with their ancient culture. Education should
be provides not only for the necessity of protecting
forest habitats in order to ensure the survival of
sloth bear, but also for highlighting the benefits to
people in protecting and managing valuable re-
sources. Sloth bear must be included as a key species
in ongoing awareness campaigns. Local people,
Joint Forest Management Committees, Eco-Devel-
opment Committees, Eco-Clubs and school chil-
dren should be sensitized about sloth bear
542
Vikas Kumar et alii
conservation. Policy makers, judiciary and enforce-
ment agencies may be sensitized on Wildlife crime
and law enforcement. Good quality audio-visual
materials and collaterals (posters, brochures, stick-
ers, etc.) in local language may be produced and dis-
tributed. Awareness campaign should focus on
highlighting damagers in collecting the minor forest
produce from the areas where bears have their dens.
VII. Legislation and Policy
Apart from the awareness and involvement of
local people, the administrative reforms are also
required for effective conservation of bears and
habitat. Despite an array of Policies and Legislation,
conservation efforts for sloth bear and its habitat
have faced limitations due to want of site specific
policies or flexibility in adaptation of existing
policies.
CONCLUSION
Some of the recommendations proposed by
stake holders to control poaching/hunting of bears
included: (i) creating awareness and using local
communities to cub bear hunting/poaching for the
illegal trade in bear parts or live cub trade; and (ii)
strengthening existing network of informers, and
various law enforcing agencies, including monitor-
ing of wildlife crimes at Inter-State check posts and
international borders. To reduce bear-human inter-
actions, the following were recommended: (i)
awareness creation on bear behaviour and the phi-
losophy of co-existence in addition to strengthening
of indigenous conflict reduction measures to reduce
crop and livestock depredation by bears; and (ii)
strengthening the conflict management teams with
equipment, training, and capacity building and im-
provement in the current mechanism of assessment
of economic losses of crop /livestock depredation
by bear and other wildlife. For bear habitat man-
agement the recommendations were to: (i) continue
protection to bear habitats and prevent habitat loss
due to conversion for agriculture/ horticulture and
developmental projects; (ii) restore degraded bear
habitats through existing government programmes
using local communities; and (iii) identify critical
bear habitats and corridors outside PA network and
manage them as Community or Conservation
Reserves with approval and support from local
communities. Similarly, recommendations for re-
search, capacity building, conservation educate and
legislation and policy have been made.
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Biodiversity Journal, 2014, 5 (4): 545-555
Biodiversity of Sudan: between the harsh conditions, political
instability and civil wars
Ahmed A.H. Siddig
PhD candidate, University of Massachusetts Amherst - Dept. Environmental Conservation, 160 Holdsworth Way/ Amherst, MA
01003-9285 U.S.A.; email: asiddig@eco.umass.edu
ABSTRACT More than 90% of the area of Sudan is classified as desert and semi-desert ecosystems, and
desertification is spreading with global climatic changes. Also the country is suffering from
60 years of chronic civil wars and instability. Consequently these situations have severely
affected the status and trend of biological diversity of the country to critical thresholds (i.e.
extinction) as many reports show. Improved knowledge of the current status of biodiversity in
response to such conservation challenges is critically important. In this review, my aim is to
highlight the recent conservation challenges of Sudan as they relate to desertification and civil
wars, and to look at the big picture of the impacts of these challenges to biodiversity conser-
vation in Africa. I then present examples of urgent management interventions and research
needs for better biodiversity conservation. The primary message of this paper is to confirm the
possibility of making conservation actions in these vulnerable areas. It is never too late as long
as there is peace and willingness. This framework could be a model to tackle and analyses bio-
diversity conservation issues in similar cases in the region.
KEY WORDS Africa; Biodiversity conservation; desertification; dry-lands; political instability; Sudan.
Received 17.10.2014; accepted 11.12.2014; printed 30.12.2014
INTRODUCTION
The news coming from Sudan is always about
civil war, political conflicts, awful statistics about
the refugees and displaced people and rarely opti-
mistic. In addition to the political instability, envi-
ronmentally the country is one of the most fragile,
dry and desertified areas in Sub-Saharan Africa,
which leads to high vulnerability to global climatic
changes and extreme events such as drought and
flooding (I.P.C.C., 2013). The United Nations Con-
vention on Combating Desertification (U.N.C.C.D.)
defined dry lands (arid, semi-arid and diy sub-humid
zones) as areas other than polar and sub-polar
regions in which the aridity index (i.e. the ratio of
annual precipitation to potential evapo-transpiration)
falls within the range of 0.05-0.65 (U.N.C.C.D.,
1994). According to this definition, about 93% of
the area of the country is classified as dryland (Table
1), which extends from hyper arid and arid zones in
the north to the semi-deserts in the middle to low
rainfall woodlands savanna in the deep south and
south east (Goda, 2007; Mustafa, 2007).
In addition to the dominant harsh conditions
there are some areas with unique ecological condi-
tions such as mountains, the Nile strip and wetlands
depressions. These areas support vegetation com-
munities and natural habitats that are critical to
maintaining biological diversity, particularly
wildlife and forest resources (Mukhtar & El
546
Ahmed A. H. Siddig
Wakeel, 2002). The forest resources in Sudan were
estimated by F.A.O. in 1990 to be about 19% of the
total area of the northern part of the countiy, but the
current report of U.S.A.I.D. in 2012 showed the
total forested areas of the country have been re-
duced substantially to about 11.6 % (Fig. 1).
Despite the habitat loss and degradation, these
forests are still playing vital enviromnental roles in
biodiversity conservation and combating desertifi-
cation as well as supporting the livelihood of local
communities. For instance the forest products con-
sumption survey conducted by the Forest National
Aridity Zone
Ecosystem type
Area
(Square Km)
% (Area of
the Sudan)
Annual
Rainfall (mm)
Aridity Index
(R=P/PET)
Hyper-arid
Desert
776000
41
<20
<0.05
Arid
Semi-desert
630000
33
20 - 100
0.05-0.20
Semi-arid
Grassland Savanna
340000
18
100-300
0.21-0.50
Dry sub -humid
Low rainfall
woodland Savanna
65000
3
300 - 500
0.51-0.65
Sub-tropic
High rainfall
woodland Savanna
70000
4
500 - 800
>0.65
Total
1881000
100
Table 1. Classification and extent of dry lands in Sudan adapted from Ayoub (1998), Mustafa (2007) and Badri (2012).
Figure 1 . The location of Sudan in Africa (left). The map of land cover showing the ecological gradients from the desert in the
north to rainy savannah in the deep south (right). The area of the country divided between 50.7% as desert, 13 % agricultural
lands, 12.6 % grass lands, 10% forests cover, 1 % Water resources. ~ 1% others (i.e. urban areas). Adapted from F.A.O. (2012).
Biodiversity of Sudan: between the harsh conditions, political instability and civil wars
547
Corporation (F.N.C.) in 1995 showed that forests
are the main sources of sawn timber, round poles,
building materials and 87.5% of energy (fuel wood)
to the country. Also about 100 indigenous trees
species provide direct food, oil, honey, fruit, fodder,
gum, fiber, medicine, and tannin agents to the peo-
ple (Badi, 2004). Takona (1999) and Siddig &
Abdellhameed (2013) emphasized the great socioe-
conomic, cultural and heritage values of biodiver-
sity of Sudan, and the value of local markets based
on wildlife products, forest products and fibers craft-
ing materials as an employment opportunity for
many people, especially in rural areas.
Although there are a few efforts by local govern-
mental agencies and NGOs, there are many critical
challenges facing biodiversity of Sudan. First, po-
litical instability and civil wars led the country to
lose about 70% of its biodiversity that was concen-
trated in the southern part, as it became independent
state in 2011 as republic of South Sudan. Severe
wars continue in about 50% of the rest of the coun-
try (8 states out of 15). Second, the combination of
socio-economic (e.g. food insecurity and refugees)
and global environmental factors (e.g. climate
change, drought and desertification) plus the lack
of integrated plans exacerbate the decline of biolog-
ical diversity of the country to critical thresholds
(i.e. extinction). The need to know the current status
of biodiversity in response to such complex politi-
cal and environmental challenges is critically
important. Nimir, (1995), Takona, (1999), Funk et
al. (2011) and Badri (2012) pose many logical
questions on this topic. I suggest that the most im-
portant questions include: What is the current state
of biodiversity of the country in the light of these
wars and harsh conditions? What and where are the
hot spots of conservation? What are the subsequent
challenges facing biodiversity? And most impor-
tantly, how can these challenges will be solved?
This review comes to bring attention to the
impacts of wars combined with harsh conditions on
biodiversity as regional theme with a particular case
of Sudan after July 2011 based on recent govern-
mental and international agencies reports working
in Sudan as well as the domestic literature. The spe-
cific aims of this paper are two-fold. First, I display
and diagnose the most serious challenges of biodi-
versity conservation in the country based on my
point of view. Second, I present a vision of solutions
as a suggested framework for biodiversity conser-
vation, including a top ten management strategies
and urgent research needs.
CONSERVATION CHALLENGES
The critical challenges facing biodiversity in
Sudan are similar to elsewhere in the continent, and
have been listed in Takona (1999), Goda (2000),
Abdelhameed & Nimir (2007), Nur (2007), U.N.E.P.
(2007), and Badri (2012). Although I generally agree
with these previous studies about these problems, I
argue that political conflicts and civil wars is a chal-
lenge that substantially affects everything in the
country including biodiversity. In the following
points I show how continuous conflicts and unrest
directly impact biodiversity conservation:
Species loss and mass extinctions
Almost 60 years of violence led the country to
lose its southern part, and continues in more than
50% of the rest of the rest of the country (9 states
out of 17). In addition, there are intermittent mili-
tary tensions in the border between Sudan and
South Sudan from time to time. Consequently, hun-
dreds of individuals of many taxa have been killed
as a direct effect of shootings and fire set by fight-
ers. Also, several species (e.g. Gazelles and Ostrich)
have declined due to overhunting by the militants
who use them as a primary food source in the
woods. Recent IUCN (2013, e.g. Tables 5) Tables
of endangered species indicate the absence of infor-
mation for about 114 animals’ species (i.e. data
deficit) and 127 species reported as threatened,
including 19 plants and 108 animals (16 mammals,
18 birds, 3 reptiles, 21 fishes and 50 invertebrates).
Many ecologically important species went extinct
since 1980s or are thought to be extirpated from
their natural territories in Blue Nile, South Darfur
and the Nuba mountains regions. Species endan-
gered because of these conflicts and other stressors
(e.g. drought) include top predators: cheetah,
Acinonyx jubatus Schreber, 1775; African lion,
Panthera leo Linnaeus, 1758; greater spotted eagle,
Aquila clanga Pallas, 1811; imperial eagle, Aquila
heliaca Savigny, 1809; houbara bustard, Chlamy-
dotis undulata (Jacquin, 1784); and lesser kestrel,
Falco naumanni J.G. Fleischer, 1818. Herbivorous
on the endangered list are Hippopotamus, Hip-
548
Ahmed A. H. Siddig
popotamus amphibius Linnaeus, 1758; Barbary
sheep, Ammotragus lervia Pallas, 1777; Dorcas
gazelle, Gazella dorcas Linnaeus, 1758; red-
fronted gazelle, Gazella rufifrons Gray, 1846;
Soemmerring’s gazelle, Gazella soemmerringei
Cretzschmar, 1826; African elephant, Loxodonta
africana Blumenbach, 1797; and African spurred
tortoise, Geo chel one sulcata (Miller, 1779), as well
as several bats like Trevor’s free-tailed bat, Mops
trevori (Allen, 1917); horn-skinned bat, Eptesicus
floweri (de Winton, 1901)', and lappet-faced vulture,
Torgos tracheliotos (Forster, 1791) (Badri, 2012).
Habitat loss and fragmentation
Habitat loss and fragmentation due to excessive
deforestation and agricultural expansion in forest
lands. The Sudanese Forest National Corporation
(F.N.C.) estimated that vast forested areas of the
sub-humid zones in southern Darfur and Kordofan
have been cleared by refugees and displaced people
for use as fuel wood and building poles. Approxi-
mately 1 million hectares was cut down during
2005-2010 in both Sudan and South Sudan (F.A.O.,
2005; Gaafar, 2011). Also according to the U.N.
mission in Sudan, millions of people from both Su-
dans have become internally displaced and refugees
as a direct impact war, surviving hard conditions
and depending largely on the already poor forests
for shelter and livelihood.
Insufficient governmental support
For decades, the government’s major concern
always is to deal with wars. There is not enough
government effort or budget allocated to develop
conservation programs. It is no secret in Sudan that
for decades, the budget of the ministries of defense
and interior is about 50-60% of the total, with the
rest divided among more than 25 ministries.
Furthermore, the latest trends in international arms
transfers showed that Sudan is classified among the
top three African countries in weapons imports,
after Algeria and Morocco, receiving 9% of the total
continent’s imports (Wezeman & Wezeman, 2014).
These numbers show the priorities of the govern-
ment, and why ministries like environment and
physical development, higher education, and
science and technology receive less than 1% of the
total budget annually.
Redundant and weak institutions
Redundant and weak institutions are responsi-
ble for managing natural resources and enforcing
conservation policies. It is surprising that many
ministries are formed to accommodate opposition
and former militia leaders who agree to partici-
pate in the government and not because of the
technical need for these ministries. Thus the is-
sues of biodiversity are divided among at least 5
ministries and unfortunately none of them is fully
functional. For example it is primarily follow to
Ministry of the Environment and Physical Devel-
opment, but it has redundancies with the Ministry
of Agriculture (especially at the state level),
Forest National Corporation, the Higher Council
of the Environment and Natural Resource and
Wildlife Protection Administration in the Ministry
of Interior.
Data deficits
A general problem in Sudan is information
gaps in almost all sectors, particularly the current
biodiversity status and geographical distribution
(What is where? What are the trends?). For exam-
ple, there are no current detailed studies about the
state of biodiversity of some important ecosystems
such as Blue Nile state (e.g. Al-Angesena area)
and South and West Darfur states (e.g. Radom
National park). Because of the unsecure condi-
tions, it is not surprising that the data collection
(e.g. species diversity) for conservation (e.g.
habitat restoration) is extremely rare and some-
times impossible. This shortage of information
makes conservation planning haphazard and inter-
ventions cannot even begin.
Accelerating natural disturbances
Desertification is a familiar scenario in almost
70% of the country and one of the biggest chal-
lenges not only because of its fast annual creeping
rate but also because it is encroaching on vast
habitat areas (Table 1). The high rate of deforesta-
tion, soil erosion, forest fires and few reforestation
efforts are primary drivers of this phenomenon. In
addition, the I.P.C.C. 5th report classified Sudan as
one of the most vulnerable spots to climatic changes
since the country is at the defense line of the sub-
Biodiversity of Sudan: between the harsh conditions, political instability and civil wars
549
Saharan region and has high deforestation rates.
Consequently extreme events such as drought,
flooding and fire are likely to increase severely
(Badri, 2012). Conflicts result in more stochastic
deforestations and unplanned use of natural re-
sources which ultimately increase the risk of ero-
sion and desertification.
Absence of local communities in establishing
Absence of local communities in establishin-
gand adopting participatory conservation projects.
Community involvement varies from place to
another, but for the time being the general public,
is concerned more about safety, peace, poverty
alleviation, and food security rather than conserving
biodiversity.
Political restrictions
Political restrictions from the government over
the NGOs working in environmental fields. Due to
these tensions some NGOs are having difficulties
implementing their conservation projects because
the government wants them to do it according to its
agenda which is not necessarily the same as the
NGO’s plans.
THE BIG PICTURE OF BIODIVERSITY
CHALLENGES IN AFRICA
The truth is that the circumstances (i.e. civil
wars and instability) threatening the biodiversity of
Sudan occur elsewhere, not only in neighboring
countries (e.g. South Sudan, Libya and Central
Republic of Africa) but also in the majority of the
African countries (e.g. Mali and Somalia). Unfor-
tunately, political instability, spreading wars and
chronic conflicts, millions of refugees and displaced
people, severe levels of poverty and low education
are the largest common denominator among most
countries of the region (Swatuk, 2007; Nur, 2007).
Furthermore, these countries have weak conserva-
tion institutions with no clear plans aggravated by
budget issues. Because conservation in general
needs committed governments, people living in a
safe and healthy environment, and available re-
sources, it is not surprising that issues of biodiver-
sity conservation are a low priority in Africa.
The other dimension of this dilemma is that we
do not know when these decades of unrest and
conflicts are going to stop (though the reasons
behind them are well known) so that development
can begin. Meanwhile, the consequences of such
deterioration of biodiversity in African countries
on the global environment and biodiversity
become more severe and uncertain. For instance,
U.N.E.P. (2013) reported that the globally impor-
tant and richest tropical areas in Africa such as
Lake Victoria, Congo basin and the Nile fall in
regions where conflicts have raged for decades
and consequently no detailed biodiversity updates
or related environmental data are available. The
ecological significance of this area is not limited
to global water budget and winter habitat for
several western migratory birds. The region is also
considered an important sink for carbon dioxide,
thus significant to the global carbon budget and all
global climate change (U.N.E.P., 2006).
While the governments and the oppositions in
countries like Mali, Libya, Egypt, Somalia and
Sudan are so busy in fighting each other and allo-
cating most resources and efforts to this, appar-
ently they have forgotten to be united against
drought and desertification as the biggest enemy
these countries and their people have ever faced.
The region has the most severe deforestation
worldwide, since vast areas being cleared by
millions from local communities who were forced
by wars, poverty and lack of development to use
forests as their only source for shelter, livelihood,
energy, and building materials. There is much to
lose: more than 70% of the African tropical forests
are located in Democratic Republic of Congo,
Rwanda, Burundi, Central African Republic,
Sudan and South Sudan, where deforestation re-
lated to conflicts is happening every day (Mon-
tagnini & Jordan, 2005).
It is important to mention the influences of this
continental unrest on the ability of international
partners (e.g. U.N.E.P., U.N.D.P., W.W.F., World
Bank, U.S.A.I.D., Conservation International, and
WCS) to continue funding biodiversity and envi-
ronmental conservation projects in Africa. Not only
is there the direct risks of performing field work or
wasting money, but part of this discouragement is
because it is very unlikely that conservation plans
will achieve the goals of the projects in a sustain-
able manner.
550
Ahmed A. H. Siddig
Despite this dark picture of biodiversity in
Africa, there are a couple of bright spots. There is
tremendous progress in some countries such as
South Africa, Kenya and Tanzania whom just
passed through a long history of similar political
tragedies but ended up as successful stories. South
Africa, after years and years of violence, is a good
example of how stability can make development
possible. Among several paths of reforms, biodiver-
sity conservation was launched following simple
principles based on strong governmental authority
and involvement of universities and research
centers, local communities and NGOs in planning
and management of natural resources. By 2012,
official South African reports stated that 9.3 million
people come to the country from all over the world
for wildlife and ecotourism, which is a great achieve-
ment in biodiversity conservation.
My second example is Kenya that came a long
way from crises to become the largest center of
international and regional environmental organiza-
tions in the continent. ‘Those trees make Kenya,
Kenya!’ is a familiar slogan to Kenyans and peo-
ple who visit Kenya. It represents the vision of the
country regarding the environment and indicates
awareness and adoption by local communities.
Establishing community based-ecotourism orga-
nizations is an impressive and creative example
that shows what can be done when a committed
government works together with responsible
NGOs and engaged citizens.
Let me conclude by mentioning the interesting
lesson of Tanzania in biodiversity conservation and
its significance in stabilizing the economy of the
country. There is no doubt that Tanzanian govern-
ment, with local and international partners, has
worked very hard to develop the current working
plan for managing protected areas and positioning
them as a primary source of income to the country.
This wonderful model of managing natural re-
sources is not only a plan for biodiversity conser-
vation, but also made Serengeti, Arusha and other
12 national parks among top tourism areas in the
world. The Tanzanian government announced in
2013 that the country has joined the club of 1-
million wildlife tourists per year, which is a big
achievement. There are also other encouraging
attempts by few countries including Zimbabwe,
Botswana, Namibia, and Zambia who are relatively
stable with well-developed biodiversity plans.
TOP TEN PROPOSALS FOR BETTER
BIODIVERSITY CONSERVATION
The big message I want to convey by this paper
is that conservation action is still possible. It is
never too late as long as there are peace, stability,
willingness, and overall the governmental commit-
ments and engaged citizens and NGOs, no matter
how few the resources. Countries can maximize the
use of land resources for the benefit of people at the
same time as aiming towards sustainable biodiver-
sity conservation. Consistent with this belief and
drawing from success stories mentioned above and
call by recent reports e.g. U.N.E.P. & I.E.S. (2007)
and Badri (2012), I suggest some strategies (Fig. 2)
to improve the existed efforts. These would be a
great start towards better biodiversity conservation
in Sudan as well as elsewhere in the region where
conflicts and unrest continue.
Management strategies
1. Governance and Government commitment
towards natural resources conservation by support-
ing annual budgets and strengthening the institu-
tions that formulate and implement the conservation
plans with systematic monitoring and evaluation
protocols.
2. Improving environmental educational
programs especially at secondary and higher
education levels by addressing the recent globally
important issues (e.g. climate change, endangered
species) as annual updates in the curriculum. More
broadly, major needs of the education system of
Sudan are strengthened polices, curriculum
reforms to match international trends (e. g. millen-
nium goals), training of faculty (teachers) and
assistant staff, and improved government commit-
ment and funding. I urge adoption of some inter-
national (similar educational models) standards
such as quality assurance systems that include
strict monitoring and evaluation system of the edu-
cational process.
3. Adoption of research and scientific methods
to identify conservation priority areas (e.g. ecosys-
tem level vs. population level) but also select
among many adaptation strategies (e.g. water har-
vesting vs. enclosures for habitat restoration).
Biodiversity of Sudan: between the harsh conditions, political instability and civil wars
551
A proposed framework for environmental conservation in Sudan
Stakeholders Inputs
A
V
Stakeholders
Gov. agencies
Universities
Research centers
N*GOs
Local communities ... etc.
Management
strategies
Assess needs/ vulnerabilities
(Existing + expected)
>
f
Develop working plans
1
Evaluate strategies
• Ecological
• Human
• Management
\
Recommended
Action(s)
1
1
1
Implementation
>
Monitoring
Figure 2. A proposed framework for environmental conservation in Sudan based on the role of the government
in initiating research and management plans with consideration of environmental stakeholders.
4. Use of technology in management planning
such as remote sensing, GIS, radio collars, camera
traps, and acoustic monitoring to improve manage-
ment and inform decision makers.
5. Adoption of long-term monitoring programs
by focusing on specific focal ecosystem indicators
(e.g. abundances, composition and richness) and
key climatic variables (e.g. amount and length of
rainy season) at pennanent plots across the country.
These monitoring data will be good indications not
only for detecting current conditions and trends, but
also could alert managers to early warning signals
of ecosystem change.
6. Involvement of indigenous communities and
nongovernmental stakeholders in conservation
planning and implementation. This community
involvement could be achieved by using a citizen
science approach that can play two roles at once.
While involvements of local communities will
likely increase the awareness about certain environ-
mental issues (e.g. risk of deforestation) it could be
a cost-effective way to collect biodiversity data
such as species occupancy information.
7. Capacity building, especially for natural re-
sources mangers, focuses on improving awareness
for the reasons to protect biodiversity, identifying
hot spots, and building monitoring skills and a
documentation system for conservation projects.
8. Enforcing and updating legislation so that
conservation efforts are based on the power of law.
One sad example though is that National park like
Radom is the biggest protected area in the country
552
Ahmed A. H. Siddig
but most of its area is dominated by drug cartels
farming activates; furthermore there is no gover-
nment authority inside the park to take actions.
9. Strengthen networking and international part-
nerships with powerful agencies such as Wildlife
Conservation Society (W.C.S.), World Wildlife
Fund (W. W.F.), and Nature Conservancy and others
to take advantage of their experience in conserva-
tion elsewhere.
10. Activating the commitments of Sudan in in-
ternational environmental conventions (e.g. United
Nations Convention on Environment and Develop-
ment, U.N.C.E.D., United Nations Framework
Convention on Climate Change, U.N.F.C.C.C.,
Convention of Biological Diversity, C.B.D., Con-
vention on international Trade in Endangered
Species of Wild Fauna and Flora (C.I.T.E.S.) and
protocols (e.g. Kyoto and Ramsar) and following
national action guidelines.
Urgent research needs
My suggestions for management interventions
emphasize the adoption of research and scientific
approaches. I believe that research must play a key
role in the next era of conservation biology in
Sudan. Research would diagnose major causes of
the deterioration of biodiversity and reveals the hot
spots of decline during the past. In addition, re-
search will establish baseline information, identify
priorities, and inform future management and in-
vestment of resources.
Although the importance of research and
science-based decisions has been urged by many
authors and reports previously (e.g. Abdelhameed,
2007; Zakialdeen, 2009; Funk et al., 2011), like all
things in Sudan, research has encountered many
obstacles ranging from funding, to weak institu-
tions and facilities, to absence of master plans, to
research capacity (e.g. training). Identifying the
most pressing research questions will help to focus
limited resources. Based on the work of Sutherland
et al. (2009) regarding the top hundred most
important questions to conservation of global bio-
diversity, I scaled down to Sudan and adapted a list
of top ten research questions about biodiversity of
the country.
The questions are:
1. Desertification and drought
Studies on the causes of desertification are rela-
tively better and more focused than studies of strate-
gies of control. Despite these efforts there are many
research gaps at the country level such as: Where
do the greatest effects of desertification occur?
What is the encroachment rate of the desert and
where does mostly occur (i.e. how many km/yr.)?
Also, important related questions remain unan-
swered, for example: What is the frequency and du-
ration of drought periods? Are there socioeconomic
impacts of desertification and drought? What are
these impacts and where?
2. Climate change
The concern with climate change in dry lands is
how to adapt to it in the context of the myriad
problems already facing these areas. For instance,
how to allocate limited resources among many
urgent needs - for example, choosing between water
harvesting techniques or establishing refiigia in pro-
tected areas - needs to be studied and choices based
on objective (i.e. quantitative) criteria. To design
effective studies, it is important that to determine
the methods of evaluating the vulnerabilities and
effectiveness of adaptations and mitigation mea-
sures at any ecosystem.
3. Biodiversity , population dynamics and
conservation hot spots
There is an absence of biodiversity information
in Sudan; the I.U.C.N. (2013) reported zeros for
many taxa to indicate a data deficit. Therefore, to as-
sess the conservation status of species and to make
a baseline for any further questions, we need to know
who is where and how many of them are there, par-
ticularly at the protected areas. For endangered
species, we need to assess the status and likelihood
of extinction by conducting a population viability
analysis (PVA), a widely adopted technique in con-
servation biology (Lindenmayer et al., 1993; Vie et
al., 2009). Additional key studies that relate conser-
vation and populations dynamics include studies of
population characteristics other than abundance. For
example, fecundity, age classes and sex ratio data,
especially for threatened species, are keys to under-
standing the population dynamics.
Biodiversity of Sudan: between the harsh conditions, political instability and civil wars
553
Understanding how human activities (e.g. defor-
estation by refugees), environmental (e.g., fire) and
biological (e.g., disease) disturbances impact popu-
lations, communities and metapopulation process
are also important.
4. Forest ecology , wetlands and habitat as-
sessment
Issues like seed germination and natural regen-
eration of some threatened trees species such as
a desert date (. Balanites aegyptiaca Del.) and
Boswellia papyrifera Del. are of great concern and
should be a priority area of research. Also there is
an absence of studies in important areas like the
temporary wetlands and flood plains of the Nile.
These are thought to be rich ecosystems supporting
several fauna and flora species as well as an essen-
tial source of livelihood to millions of people living
at the Nile strip and tributaries.
5. Ecological modeling and forecasting
Modeling, simulations and other statistical tech-
niques can be employed to craft very sophisticated
ecological questions (e.g. what if) and to improve our
understanding about possible future scenarios. Mod-
eling techniques can also integrate data and predic-
tions over large spatial scales (i.e. landscape level).
6. Environmental education
I believe that education is the right way to start
making real changes in biodiversity conservation in
the country. However, the current education system
is broken and needs to be reformed on scientific
basis starting by asking questions like: Does our
education meet standards at the levels of internatio-
nal criteria (e.g. international education polices of
the U.N.E.S.C.O.)? How could we develop a
quality assurance system for higher education
institutions generally in Sudan in a cost-effective
way? I think by answering these questions we can
make sure our environmental education meets the
international quality standards in higher education
with a monitoring and evaluation system.
7. Environmental risk assessments
Despite the political instability and unrest,
Sudan has witnessed some developmental projects
such new dams, highways and establishment of
urban centers. The call here is that biodiversity and
risk assessments studies should be considered when-
ever similar projects are being planned (El-
Meghraby, 2009). As violence and conflicts continue
in many parts of the country, there is a need to know
what exactly the effect of these wars is on biodiver-
sity. I suggest that knowing the effect of a particular
civil war that has a certain number of refuges on the
surrounding forest cover would be useful to predict
the future dynamics of the habitat affected by war.
CONCLUSIONS
Biodiversity is of critical importance to the
livelihood of people and is also of high ecological
value. Despite its importance, biodiversity in
Sudan, as many other resources, has been a victim
of political instability and continuous civil wars
since the 1950s. Absence of strong governance and
polices, and socioeconomic factors have contrib-
uted to this substantial deterioration. In addition, the
harsh setting, drought, desertification, flooding,
fire, habitat destruction and recent climate change
have played a great role in reducing habitats and
populations.
Despite these stressors on biodiversity and the
lack of current information about the ecosystems,
communities and populations, conservation efforts
must proceed with effective management actions.
Urgent management actions at this point should in-
clude governance and governmental commitment
(e.g. funding, facilities, policies), adoption of re-
search and improving environmental education,
adoption of technology and long-term monitoring
programs, and involving local communities and
NGOs in planning and enforcement of legislations.
The government must also stay committed to inter-
national environmental conventions and protocols
(i.e. U.N.C.E.D., U.N.F.C.C.C., C.B.D., C.I.T.E.S.),
Finally, I recommend capacity building and training
of conservation practitioners. This would have great
value especially if it is conducted in the context of
international partnerships with other prominent
conservation agencies (e.g. U.S.A.I.D., W.C.S.,
W.W.F., and The Nature Conservancy).
The research need at this point is to create the
bench marks to build upon. Not only questions
concerning species richness and abundance are
554
Ahmed A. H. Siddig
important. It is also critical to know the effects of
different disturbance factors (e.g. desertification
and human aspects) on the ecosystems, habitats and
populations. Studies investigating the role of biodi-
versity in the livelihood of local communities as
well as the role of communities in conservation
should be a priority. The Nile needs more in-depth
investigations about its faunal and floral diversity,
biogeochemistry, water chemistry and the effects of
heavy agricultural and urbanization activities on the
environment of the both banks of the Nile. Also
areas affected by the conflicts, especially where the
effects of refugees and internally displaced people
could affect the resources must be a priority of
research.
In conclusion, I believe that all researchers and
conservation biologists in Sudan share with me the
same positive feelings and responsibility about the
country’s biodiversity and resources. I hope this
work to lead to new initiatives from both the gov-
ernment agencies and conservation biologists. I
truly want this report to motivate in-depth work and
collaborative efforts that will substantially improve
the status of biodiversity in Sudan as well as be a
model for conservation in the region.
ACKNOWLEDGEMENTS
This paper came after the invitation from Har-
vard Forest (H.F.), Harvard University to give a talk
about biodiversity of Sudan - status, conservation
challenges, research needs. I do gratefully offer my
acknowledgment to Audrey Barker Plotkin - the re-
search and seminar coordinator in HF for the request
and discussion of the initial idea. Also I would like
to warmly thank Professor Aaron M. Ellison, Har-
vard Forest for his valuable comments and encoura-
gement to write this paper. Also I extend my thanks
to Islamic Development Bank (I.D.B.) for funding
my PhD research in US as well as to Harvard Forest
for providing host and space to my research.
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